Plankton Ecology of the Southwestern Atlantic pp 541-563 | Cite as
Responses of Subantarctic Marine Phytoplankton to Ozone Decrease and Increased Temperature
Abstract
Temperature and ultraviolet B radiation (UVB, 280–315 nm) are external stressors that affect organisms in mid and high latitudes in a combined way. The combined effects of both variables on natural marine phytoplankton from the Beagle Channel (Argentina) were examined during a 7-day mesocosm experiment. We tested the hypothesis that increased temperature (HT, +3 °C) will offset negative effects on phytoplankton by UVB (natural, NUVB, and high, HUVB, simulating a 60% decrease in stratospheric ozone layer thickness). The response of the entire phytoplankton assemblage, in terms of phytoplankton biomass, community composition, reactive oxygen species (ROS), lipid damage (TBARS), nonenzymatic antioxidants (α-tocopherol (αT) and β-carotene (βC)), and mycosporine-like amino acids (MAAs), was evaluated. On the first exposure day, assemblages exposed to HUVB showed a significant increase in ROS content, regardless of the temperature, while lipid damage was significantly higher at HT and HUVB. However, on day 2, lipid damage was significantly lower possibly due to the consumption of the nonenzymatic antioxidants that protected the membranes from further damage. Under normal temperature (NT) conditions, ROS concentrations were significantly lower compared with day 1, and nonenzymatic antioxidant concentrations remained high (0.025 nmol C−1 compared with 0.05 nmol C−1 at initial time). ROS increased again in HT-HUVB and in control (NT-NUVB), in coincidence with a significant increase in UVB radiation on day 4. However, the lipid damage was significantly lower in HT-HUVB than in control conditions possibly due to a higher consumption of nonenzymatic antioxidants and probably also to a higher activity of enzymatic antioxidants by the effect of the higher temperature. The same results were observed for HT-NUVB, with low lipid damage. During all experiment no significant differences were observed in carbon-normalized MAAs. After day 4, when nutrients became limiting, high temperature significantly influenced community structure, with a negative impact on diatoms and positive on phytoflagellates, independently of the UVB doses. Our results show that subantarctic phytoplankton is able to respond to a ROS increase via antioxidant response in high irradiance conditions. In addition, increased temperature and phytoplankton community composition play a central role in this response. At lower UVB doses, diatoms were able to avoid UVB lipid damage by αT and βC synthesis. However, with maximum doses, phytoflagellates showed a best UVB adaptation to high temperature conditions.
Keywords
UBVR Increased temperature Beagle Channel Phytoplankton assemblage ROS Nonenzymatic antioxidantsNotes
Acknowledgments
This research is part of the project “Combined Effects of Ultraviolet-B Radiation, Increased CO2 and Climate Warming on the Biological Pump: A Temporal and Latitudinal Study,” led by S.D. and supported by the Natural Sciences and Engineering Research Council of Canada (NSERC, SRO Grant# 334876-2005) and by a grant from the Instituto Antártico Argentino (IAA) to G.A.F. in the frame of the project “Research on Ultraviolet and Global warming effects on Biological pump Yields” (RUGBY). We want to thank Dr. Jose Carreto and Mario Carignan for providing the MAA data. We also want to thank the numerous people that helped us with the setup of the mesocosms and the experiment in Ushuaia: Sylvain Leblanc, Patrick Poulin, Alejandro Olariaga, Alejandro Ulrich, and Raúl Codina.
References
- Alley R, Berntsen T, Bindoff NL et al (2007) Climate change 2007: the physical science basis. Summary for policymakers, Intergovernmental Panel on Climate Change, GenevaGoogle Scholar
- Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–379CrossRefGoogle Scholar
- Beardall J, Stojkovic S (2006) Microalgae under global environmental change: implications for growth and productivity, populations and trophic flow. Sci Asia 32:1–10CrossRefGoogle Scholar
- Behrenfeld MJ, O’Malley R, Siegel D et al (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755CrossRefGoogle Scholar
- Bergmann T, Richardson TL, Paerl HW et al (2002) Synergy of light and nutrients on the photosynthetic efficiency of phytoplankton populations from the Neuse River Estuary, North Carolina. J Plankton Res 24:923–933CrossRefGoogle Scholar
- Bouchard JN, Roy S, Campbell DA (2006) UVB effects on the photosystem II-D1 protein of phytoplankton and natural phytoplankton communities. Photochem Photobiol 82:936–951CrossRefPubMedGoogle Scholar
- Carreto JI, Carignan MO, Daleo G et al (1990) Occurrence of Mycosporine-like Aminoacids in the red-tide dinoflagellate Alexandrium excavatum: UV-Photoprotective compounds? J Plankton Res 12:909–921CrossRefGoogle Scholar
- Carreto JI, Carignan MO, Montoya NG (2002) Short-term effects of ultraviolet radiation on the dinofagellate Alexandrium catenella. Pigment bleaching and MAAs synthesis inhibition. In: G. Arzul (ed). Aquaculture, environment and marine phytoplankton. IFREMER, Actes colloq 34:173–190Google Scholar
- Davidson AT, Marchant HJ, de la Mare WK (1996) Natural UVB exposure changes the species composition of Antarctic phytoplankton in mixed cultures. Aquat Microb Ecol 10:299–305CrossRefGoogle Scholar
- Desai ID (1984) Vitamin E analysis methods for animal tissues. Methods Enzymol 105:138–147CrossRefPubMedGoogle Scholar
- Díaz S, Nelson D, Deferrari G et al (2003) A model to extend spectral and multi-wavelength UV irradiances time series. Model development and validation. J Geophys Res. https://doi.org/10.1029/2002JD002134
- Diaz S, Camilion C, Cassiccia C et al (2006) Symposium-in-print: UV effects on aquatic and coastal ecosystems simulation of ozone depletion using ambient irradiance supplemented with UV lamps. Photochem Photobiol 82:857–864CrossRefPubMedGoogle Scholar
- Dijkman NA (2001) The regulation of photosynthesis in diatoms under dynamic irradiance. PhD thesis. Universität BremenGoogle Scholar
- Eppley RW (1972) Temperature and phytoplankton growth in the sea. Fish Bull Nat Ocean Atmos Adm 70:1063–1085Google Scholar
- Eun-Ji W, Lee Y, Han J et al (2014) Effects of UV radiation on hatching, lipid peroxidation, and fatty acid composition in the copepod Paracyclopina nana. Comp Biochem Physiol C Toxicol Pharmacol 165:60–66CrossRefGoogle Scholar
- Ferreyra GA, Mostajir B, Schloss IR et al (2006) Ultraviolet-B radiation effects on the structure and function of lower trophic levels of the marine planktonic food web. Photochem Photobiol 82:887–897CrossRefPubMedGoogle Scholar
- Folt CL, Chen CY, Moore MV et al (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877CrossRefGoogle Scholar
- Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717CrossRefGoogle Scholar
- Garcia-Pichel F (1994) A model for shelf-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717CrossRefGoogle Scholar
- Giannuzzi L, Krock B, Crettaz MC et al (2016) Growth, toxin production, active oxygen species and antioxidants responses of Microcystis aeruginosa (Cyanophyceae) to temperature stress. Comp Biochem Physiol C189:22–30Google Scholar
- González PM, Malanga G, Puntarulo S (2015) Cellular oxidant/antioxidant network: update on the environmental effects over marine organisms. Open Mar Biol J 9:1–13CrossRefGoogle Scholar
- Häder DP, Kumar HD, Smith RC et al (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285CrossRefPubMedGoogle 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 Biol 101:196–205CrossRefGoogle Scholar
- Halac SR, Guendulain-García SD, Villafañe VE et al (2013) Responses of tropical plankton communities from the Mexican Caribbean to solar ultraviolet radiation exposure and increased temperature. J Exp Mar Biol Ecol 445:99–107CrossRefGoogle Scholar
- Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Clarendon, OxfordGoogle Scholar
- Hare CE, DiTullio GR, Popels LC et al (2007) Effects of changing continuous iron input rates on a Southern Ocean algal assemblage. Deep-Sea Res I 54:732–746CrossRefGoogle Scholar
- Häubner N, Sylvander P, Vuori K et al (2014) Abiotic stress modifies the synthesis of alpha-tocopherol and beta-carotene in phytoplankton species. J Phycol 50:753–759CrossRefPubMedGoogle Scholar
- Helbling EW, Villafañe VE, Holm-Hansen O (1994) Effects of Ultraviolet Radiation on Antarctic Marine Phytoplankton Photosynthesis with Particular Attention to the Influence of Mixing. In: Weiler CS, Penhale P (eds) Ultraviolet radiation in Antarctica: measurements and biological effects. American Geophysical Union, Antarct Res Ser, 62:207–227Google Scholar
- Helbling EW, Banaszak AT, Villafañe VE (2015) Differential responses to the combination UVR and elevated temperature of two phytoplankton communities of the Chubut River estuary (Patagonia, Argentina). Estuar Coasts 38:1134–1146CrossRefGoogle Scholar
- Hernando M (2011) Fitoplancton de altas latitudes en condiciones de ozono disminuido. 1 ed. Editorial Académica Española, Reino Unido, p300. ISBN-10: 3846560545Google Scholar
- Hernando M, Malanga G, Ferreyra GA (2005) Oxidative stress and antioxidant defenses generated by solar UV in a subantarctic marine phytoflagellate. Sci Mar 69:287–295CrossRefGoogle Scholar
- Hernando M, Schloss I, Roy S et al (2006) Photoacclimation to long-term UVR exposure of natural Subantarctic phytoplankton communities: fixed surface incubations versus mixed mesocosms. Photochem Photobiol 82:923–935CrossRefPubMedGoogle Scholar
- Hernando M, Malanga G, Puntarulo S et al (2011) Non-enzymatic antioxidant photoprotection against potential UVBR-induced damage in an Antarctic diatom (Thalassiosira sp). Lat Am J Aquat Res 39(3):397–408CrossRefGoogle Scholar
- Hernando M, Carreto JI, Carignan MO et al (2012) Effect of vertical mixing on short-term mycosporine-like amino acids (MAAs) synthesis in the Antarctic diatom, Thalasiossira sp. Sci Mar 76(1):49–57CrossRefGoogle Scholar
- Hernando M, Schloss IR, Malanga G et al (2015) Effects of salinity changes on coastal antarctic phytoplankton physiology and assemblage composition. J Exp Mar Biol Ecol 466:110–119CrossRefGoogle Scholar
- Hideg E, Vass I (1996) UV-B induced free radical production in plant leaves and isolated thylakoid membranes. Plant Sci 115:251–260CrossRefGoogle Scholar
- Hillebrand H, Dürselen C-D, Kirschtel D et al (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
- Huertas IE, Rouco M, López-Rodas V et al (2011) Warming will affect phytoplankton differently: evidence through a mechanistic approach. Proc R Soc B 278:3534–3543CrossRefPubMedGoogle Scholar
- Ibelings BW, Kroon BMA, Mur LR (1994) Acclimation of photosystem II in a cyanobacterium and a eukaryotic green alga to high and fluctuating photosynthetic flux densities, simulating light regimes induced by mixing lakes. New Phytol 128:407–424CrossRefGoogle Scholar
- Irwin AJ, Finkel ZV (2008) Mining a sea of data: determining controls of ocean chlorophyll. PLoS One 3:e3836. https://doi.org/10.1371/Journal.pone.0003836 CrossRefPubMedPubMedCentralGoogle Scholar
- Irwin AJ, Oliver MJ (2009) Are ocean deserts getting larger? Geophys Res Lett. https://doi.org/10.1029/2009GL039883
- Janknegt PJ, van de Poll WH, Visser RJW et al (2008) Oxidative stress responses in the marine antarctic diatom Chaetoceros brevis (bacillariophyceae) during photoacclimation. J Phycol 44:957–966CrossRefPubMedGoogle Scholar
- Karsten U, Bischof K, Hanelt D et al (1999) The effect of UV radiation on photosynthesis and UV-absorbing substances in the endemic Arctic macroalga Develaraea ramentacea (Rhodophyta). Physiol Plant 105:58–66CrossRefGoogle Scholar
- Kingston-Smith AH, Foyer CH (2000) Over expression of Mn-superoxide dismutase in maize leaves leads to increased monodehydroascorbate reductase, dehydroascorbate reductase and glutathione reductase activities. J Exp Bot 51:1867–1877CrossRefPubMedGoogle Scholar
- Klisch M, Häder DP (2002) Wavelength dependence of mycosporine-like amino acid synthesis in Gyrodinium dorsum. J Photochem Photobiol B 66(1):60–66CrossRefPubMedGoogle Scholar
- Lionard M, Roy S, Tremblay-Létourneau M et al (2012) Combined effects of increased UV-B and temperature on the pigment-determined marine phytoplankton community of the St. Lawrence Estuary. Mar Ecol Prog Ser 445:219–234CrossRefGoogle Scholar
- Litchman E (2000) Growth rates of phytoplankton under fluctuating light. Freshw Biol 44:223–235CrossRefGoogle Scholar
- Longhi ML, Ferreyra G, Schloss I et al (2006) Variable phytoplankton response to enhanced UV-B and nitrate addition in mesocosm experiments at three latitudes (Canada, Brazil and Argentina). Mar Ecol Prog Ser 313:57–72CrossRefGoogle Scholar
- Malanga G, Puntarulo S (1995) Oxidative stress and antioxidant content in Chlorella vulgaris after exposure to ultraviolet-B radiation. Physiol Plant 94(4):672–679CrossRefGoogle Scholar
- Malanga G, Juarez AB, Albergheria JS et al (2001) Efecto de la radiación UVB sobre el contenido de ascorbato y radical ascorbilo en algas verdes. In: Alveal K, Antezana T (eds) Sustentabilidad de la Biodiversidad, un problema actual, bases científico-técnicas, teorizaciones y proyecciones. Universidad de Concepción, Concepción, pp p389–p398Google Scholar
- McDowell RE, Amsler CD, Dickinson DA et al (2013) Reactive oxygen species and the Antarctic macroalgal wound response. J Phycol 50:71–80CrossRefPubMedGoogle Scholar
- Meehl GA, Stocker TF, Collins WD et al (2007) Global climate projections. In: Solomon S, Qin D, Manning M et al (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, UK/New YorkGoogle Scholar
- Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45(3):569–579CrossRefGoogle Scholar
- Mittler R (2002) Oxidative stress, antioxidants, and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
- Moisan JR, Moisan TA, Abbott MR (2002) Modelling the effect of temperature on the maximum growth rates of phytoplankton populations. Ecol Model 153:197–215CrossRefGoogle Scholar
- Montagnes DJS, Franklin DJ (2001) Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnol Oceanogr 46(8):2008–2018CrossRefGoogle Scholar
- Montagnes DJS, Berges JA, Harrison PJ et al (1994) Estimating carbon, nitrogen, protein, and chlorophyll-a from volume in marine phytoplankton. Limnol Oceanogr 39(5):1044–1060CrossRefGoogle Scholar
- Moreau S, Mostajir B, Almandoz GO et al (2014) Effects of enhanced temperature and ultraviolet B radiation on a natural plankton community of the Beagle Channel (Southern Argentina): a mesocosm study. Aquat Microb Ecol 72:155–173CrossRefGoogle Scholar
- Mostajir B, Demers S, de Mora S et al (1999) Experimental test of the effect of ultraviolet-B radiation in a planktonic community. Limnol Oceanogr 44:586–596CrossRefGoogle Scholar
- Mostajir B, Demers S, de Mora SJ et al (2000) Implications of UV radiation on the food web structure and consequences on the carbon flow. In: de Mora SJ, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 310–320CrossRefGoogle Scholar
- Neale PJ, Helbling EW, Zagarese HE (2003) Modulation of UVR exposure and effects by vertical mixing and advection. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems, Comprehensive series in Photochemical and Photobiological Sciences. The Royal Society of Chemistry, Cambridge, pp 107–134Google Scholar
- Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Res Plant Physiol Plant Mol Biol 50:333–359CrossRefGoogle Scholar
- Noiri Y, Kudo I, Kiyosawa H et al (2005) Influence of iron and temperature on growth, nutrient utilization ratios and phytoplankton species composition in the western subarctic Pacific Ocean during the SEEDS experiment. Prog Oceanogr 64:149–166CrossRefGoogle Scholar
- Orce LV, San Román NA, Paladini A et al (1997) Multiple regression fit. Latitudinal UVR-PAR measurements in Argentina: extent of the ‘ozone hole’. Glob Planet Chang 15:113–121CrossRefGoogle Scholar
- Polle A, Rennenberg H (1994) Photooxidative stress in trees. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and ameloration of defence systems in plants. CRC Press, London, pp 199–218Google Scholar
- Rastogi RP, Incharoensakdi A (2014) UV radiation-induced biosynthesis, stability and antioxidant activity of mycosporine-like amino acids (MAAs) in a unicellular cyanobacterium Gloeocapsa sp. CU2556. J Photochem Photobiol B 130:287–292CrossRefPubMedGoogle Scholar
- Rijstenbil JW (2002) Assessment of oxidative stress in the planktonic diatom Thalassiosira pseudonana in response to UVA and UVB radiation. J Plankton Res 24:1277–1288CrossRefGoogle Scholar
- Rose JM, Feng Y, Gobler CJ et al (2009) The effects of increased pCO2 and temperature on the North Atlantic Spring Bloom. II. Microzooplankton abundance and grazing. Mar Ecol Prog Ser 388:27–40CrossRefGoogle Scholar
- Sarmiento J, Slater RD, Barber R et al (2004) Response of ocean ecosystems to climate warming. Global Biochem Cycles 18:1–23CrossRefGoogle Scholar
- Scheiner SM (2001) MANOVA: multiple response variables and multispecies interactions. In: Scheiner G (ed) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, OxfordGoogle Scholar
- Shick JM, Lesser MP, Jokiel PL (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Glob Chang Biol 2:527–545CrossRefGoogle Scholar
- Sobrino C, Neale PJ (2007) Short-term and long-term effects of temperature on photosynthesis in the diatom Thalassiosira pseudonana under UVR exposures. J Phycol 43:426–436CrossRefGoogle Scholar
- Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitt Int Ver Theor Angew Limnol 9:1–38Google Scholar
- Van Leeuwe MA, van Sikkelerus B, Gieskes WWC et al (2005) Taxon-specific differences in photoacclimation to fluctuating irradiance in an Antarctic diatom and a green flagellate. Mar Ecol Prog Ser 288:9–19CrossRefGoogle Scholar
- Vernet M (2000) Effects of UV radiation on the physiology and ecology of marine phytoplankton. In: De Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge Environ Chem Ser, 10, Cambridge University Press, Cambridge, pp 237–278Google Scholar
- Villafañe VE, Helbling EW, Holm-Hansen O et al (1995) Acclimatization of Antarctic natural phytoplankton assemblages when exposed to solar ultraviolet radiation. J Plankton Res 17:2295–2306CrossRefGoogle Scholar
- Villafañe VE, Sundback K, Figueroa FL et al (2003) Photosynthesis in the aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 357–397 (Chapter 2)Google Scholar
- Wada N, Sakamoto T, Matsugo S (2015) Mycosporine-like amino acids and their derivatives as natural antioxidants. Antioxidants 4(3):603–646CrossRefPubMedPubMedCentralGoogle Scholar
- Wängberg SÅ, Garde K, Gustavson K et al (1999) Effects of UV-B radiation on marine phytoplankton communities. J Plankton Res 21:147–166CrossRefGoogle Scholar