Pigment concentration, photosynthetic performance, and fatty acid profile of sub-Antarctic brown macroalgae in different phases of development from the Magellan Region, Chile

  • Marco Aurélio Ziemann dos SantosEmail author
  • Samantha Coelho de Freitas
  • Lucas Moraes Berneira
  • Andres Mansilla
  • Maria Soledad Astorga-España
  • Pio Colepicolo
  • Claudio Martin Pereira de Pereira


Macroalgae Durvillaea antarctica, Lessonia flavicans, and Macrocystis pyrifera in distinct development phases from the ecoregion of Magellan (Chile) were analyzed by pulse amplitude modulated fluorometry under eight irradiation conditions (11 to 490 μmol photons m−2 s−1). Pigmentation was assessed by UV/Vis spectrophotometry (400 to 700 nm), and fatty acid (FA) profile was determined by gas chromatography using the standards of their respective methyl esters (0.625 to 20 mg mL−1). Photosynthetic efficiency had significant differences for L. flavicans (0.31 ± 0.01 to 0.38 ± 0.01 μmol e m−2 s−1 (μmol photons m−2 s−1)-1) and M. pyrifera (0.26 ± 0.02 to 0.31 ± 0.03 μmol e m−2 s−1 (μmol photons m−2 s−1)-1) for reproductive and vegetative phases, respectively. The relative maximum electron transfer rate varied significantly for L. flavicans (8.10 ± 0.84 to 12.40 ± 1.57 μmol e s−1) and M. pyrifera (6.49 ± 1.30 to 12.89 ± 1.53 μmol e s−1) in distinct development phases. Saturation irradiance analysis showed significant differences for D. antarctica, varying from 166.18 ± 14.33 (vegetative) to 132.98 ± 18.43 μmol photon m−2 s−1 (reproductive). The highest concentrations of pigments were found in reproductive M. pyrifera with 35.36 ± 0.21 of Chl a, 7.04 ± 0.93 of Chl c, and 15.75 ± 1.42 μg g−1 of fucoxanthin. Finally, the highest concentrations of total FAs were 35.24 ± 2.38% (saturated) and 22.02 ± 1.95% (monounsaturated) in M. pyrifera and 63.53 ± 3.36% (polyunsaturated) in D. antarctica. Therefore, the study showed significant differences for photosynthetic parameters and FA profiles correlating these results to the development phases of macroalgae.


Polyunsaturated Fatty acids Brown algae Photosynthetic activity Sub-Antarctic region 



This study had logistic support from the University of Magallanes and the Laboratory of Antarctic and sub-Antarctic Marine Ecosystems, Instituto de Ecología y Biodiversidad (IEB), Chile.

Funding information

The authors are grateful for the financial and fellowship support from the Brazilian research funding agencies: the National Program for Post-Doctoral Studies, Coordination for Improvement of Higher Level Personnel (PNPD-CAPES, General Program of International Cooperation PGCI-99999.002378/2015), and National Council for Scientific and Technological Development (CNPq).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2019_1777_MOESM1_ESM.docx (32 kb)
ESM 1 (DOCX 32 kb)


  1. Andersen GS, Pedersen MF, Nielsen SL, Harley C (2013) Temperature acclimation and heat tolerance of photosynthesis in Norwegian Saccharina latissima (Laminariales, Phaeophyceae). J Phycol 49:689–700CrossRefPubMedGoogle Scholar
  2. Astorga-España MS, Mansilla A (2014) Sub-Antarctic macroalgae: opportunities for gastronomic tourism and local fisheries in the Region of Magallanes and Chilean Antarctic Territory. J Appl Phycol 26:973–978Google Scholar
  3. Batista MB, Anderson AB, Sanches PF, Polito PS, Silveira TCL, Velez-Rubio MG, Scarabino F, Camacho O, Schmitz C, Martinez A, Ortega L, Fabiano G, Rothman MD, Liu G, Ojeda J, Mansilla A, Barreto LM, Assis J, Serrão EA, Santos R, Horta PA (2018) Kelps’ long-distance dispersal: role of ecological/oceanographic processes and implications to marine forest conservation. Diversity 10:1–25Google Scholar
  4. Berquin IM, Edwards IJ, Chen YQ (2008) Multi-targeted therapy of cancer by ω-3 fatty acids. Cancer Lett 269:363–377CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bi Y, Zhou Z (2016) Absorption and transport of inorganic carbon in kelps with emphasis on Saccharina japonica. In: Najafpour MM (ed) Applied photosynthesis - new progress. InTech, Riejeka, pp 111–130Google Scholar
  6. Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166CrossRefGoogle Scholar
  7. Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefPubMedGoogle Scholar
  8. Brazilian Pharmacopeia (2010) National Agency of Sanitary Vigilance, Editor FioCruz, Brasília, pp 91. Searched on 8 May 2018
  9. Buschmann AH, Pereda SV, Varela DA, Rodríguez-Maulén J, López A, González-Carvajal L, Schilling M, Henríquez-Tejo EA, Hernández-González MC (2014) Ecophysiological plasticity of annual populations of giant kelp (Macrocystis pyrifera) in a seasonally variable coastal environment in the Northern Patagonian Inner Seas of Southern Chile. J Appl Phycol 26:837–847CrossRefGoogle Scholar
  10. Colombo-Pallotta MF, García-Mendoza E, Ladah LB (2006) Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol 42:1225–1234CrossRefGoogle Scholar
  11. Connan S, Deslandes E, Gall EA (2007) Influence of day–night and tidal cycles on phenol content and antioxidant capacity in three temperate intertidal brown seaweeds. J Exp Mar Biol Ecol 349:359–369CrossRefGoogle Scholar
  12. Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences methods and applications. Springer, Dordrecht, pp 1–17Google Scholar
  13. Cruces E, Huovinen P, Gómez I (2012) Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three South Pacific kelps. Photochem Photobiol 88:58–66CrossRefPubMedGoogle Scholar
  14. Cruces E, Rautenberger R, Rojas-Lillo Y, Cubillos VM, Arancibia-Miranda N, Ramírez-Kushel E, Gómez I (2017) Physiological acclimation of Lessonia spicata to diurnal changing PAR and UV radiation: differential regulation among downregulation of photochemistry, ROS scavenging activity and phlorotannins photoprotective mechanisms. Photosynth Res 131:145–157CrossRefPubMedGoogle Scholar
  15. Dambeck M, Sandmann G (2014) Antioxidative activities of algal keto carotenoids acting as antioxidative protectants in the chloroplast. Photochem Photobiol 90:814–819PubMedGoogle Scholar
  16. Dawes C (2016) Macroalgae systematics. In: Fleurence J, Levine I (eds) Seaweed in health and disease prevention. Academic Press, New York, pp 107–148CrossRefGoogle Scholar
  17. Fariman GA, Shastan SJ, Zahedi MM (2016) Seasonal variation of total lipid, fatty acids, fucoxanthin content, and antioxidant properties of two tropical brown algae (Nizamuddinia zanardinii and Cystoseira indica) from Iran. J Appl Phycol 28:1323–1331CrossRefGoogle Scholar
  18. Fernandes F, Barbosa M, Oliveira AP, Azevedo IC, Sousa-Pinto I, Valentão P, Andrade PB (2016) The pigments of kelps (Ochrophyta) as part of the flexible response to highly variable marine environments. J Appl Phycol 28:3689–3696CrossRefGoogle Scholar
  19. Franklin LA, Forster RM (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32:207–232Google Scholar
  20. Freile-Pelegrín Y, Robledo D (2013) Bioactive phenolic compounds from algae. In: Hernández-Ledesma B, Herrero M (eds) Bioactive compounds from marine foods: plant and animal sources. Wiley, New York, pp 113–129CrossRefGoogle Scholar
  21. Fujii R, Kita M, Doe M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Mizoguchi T, Cogdell RJ, Hashimoto H (2012) The pigment stoichiometry in a chlorophyll a/c type photosynthetic antenna. Photosynth Res 111:165–172CrossRefPubMedGoogle Scholar
  22. Fukumoto R, Borlongan IA, Nishihara GN, Endo H, Terada R (2018) Photosynthetic responses to photosynthetically active radiation and temperature including chilling-light stress on the heteromorphic life history stages of a brown alga, Cladosiphon okamuranus (Chordariaceae) from Ryukyu Islands, Japan. Phycol Res 66:209–217CrossRefGoogle Scholar
  23. Galindo V, Gosselin M, Lavaud J, Mundy CJ, Else B, Ehn J, Babin M, Rysgaard S (2017) Pigment composition and photoprotection of Arctic Sea ice algae during spring. Mar Ecol Prog Ser 585:49–69CrossRefGoogle Scholar
  24. Galloway AWE, Britton-Simmons KH, Duggins DO, Gabrielson PW, Brett MT (2012) Fatty acid signatures differentiate marine macrophytes at ordinal and family ranks. J Phycol 48:956–965CrossRefPubMedGoogle Scholar
  25. Gerasimenko NI, Skriptsova AV, Busarova NG, Moiseenko OP (2011) Effects of the season and growth stage on the contents of lipids and photosynthetic pigments in brown alga Undaria pinnatifida. Russ J Plant Physiol 58:885–891CrossRefGoogle Scholar
  26. Gómez I, Huovinen P (2011) Morpho-functional patterns and zonation of south Chilean seaweeds: the importance of photosynthetic and bio-optical traits. Mar Ecol Prog Ser 422:77–91CrossRefGoogle Scholar
  27. Gómez I, Huovinen P (2015) Lack of physiological depth patterns in conspecifics of endemic Antarctic brown algae: a trade-off between UV stress tolerance and shade adaptation? PLoS One 10:e0134440CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gómez I, Ulloa N, Orostegui M (2005) Morpho-functional patterns of photosynthesis and UV sensitivity in the kelp Lessonia nigrescens (Laminariales, Phaeophyta). Mar Biol 148:231–240CrossRefGoogle Scholar
  29. Gomez I, Navarro NP, Huovinen P (2018) Bio-optical and physiological patterns in Antarctic seaweeds: a functional trait based approach to characterize vertical zonation. Prog OceanogrGoogle Scholar
  30. Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationships. Mar Ecol Prog Ser 231:67–74CrossRefGoogle Scholar
  31. Graiff A, Pantoja JF, Tala F, Thiel M (2016) Epibiont load causes sinking of viable kelp rafts: seasonal variation in floating persistence of giant kelp Macrocystis pyrifera. Mar Biol 163:190–204CrossRefGoogle Scholar
  32. Häder DP, Williamson CE, Wängberg SA, Rautio M, Rose KC, Gao K, Helbling EW, Sinhah RP, Worresti R (2015) Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem Photobiol Sci 14:108–126CrossRefPubMedGoogle Scholar
  33. Hannach G, Santelices B (1985) Ecological differences between the isomorphic reproductive phases of two species of Iridaea (Rhodophyta: Gigartinales). Mar Ecol Prog Ser 22:291–303CrossRefGoogle Scholar
  34. Harwood JL, Guschina IA (2009) The versatility of algae and their lipid metabolism. Biochimie 91:679–684CrossRefPubMedGoogle Scholar
  35. Holzinger A, Pichrtová M (2016) Abiotic stress tolerance of charophyte green algae: new challenges for omics techniques. Front Plant Sci 7:1–17CrossRefGoogle Scholar
  36. Holzinger A, Di Piazza L, Lütz C, Roleda MY (2011) Sporogenic and vegetative tissues of Saccharina latissima (Laminariales, Phaeophyceae) exhibit distinctive sensitivity to experimentally enhanced ultraviolet radiation: photosynthetically active radiation ratio. Phycol Res 59:221–235CrossRefGoogle Scholar
  37. Jin H, Li M, Duan S, Fu M, Dong X, Liu B, Wang HB (2016) Optimization of light-harvesting pigment improves photosynthetic efficiency. Plant Physiol 172:1720–1731CrossRefPubMedPubMedCentralGoogle Scholar
  38. Jones AB, Dennison WC, Stmart GR (1996) Macroalgal responses to nitrogen source and availability: amino acid metabolic profiling as a bioindicator using Gracilaria edulis (Rhodophyta). J Phycol 32:757–766CrossRefGoogle Scholar
  39. Juneja A, Ceballos RM, Murthy GS (2013) Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: a review. Energies 6:4607–4638CrossRefGoogle Scholar
  40. Kaplan F, Lewis LA, Herburger K, Holzinger A (2013) Osmotic stress in Arctic and Antarctic strains of the green alga Zygnema (Zygnematales, Streptophyta): effects on photosynthesis and ultrastructure. Micron 44:317–330Google Scholar
  41. Khoroshyy P, Bína D, Gardian Z, Litvín R, Alster J, Pšenčík J (2018) Quenching of chlorophyll triplet states by carotenoids in algal light-harvesting complexes related to fucoxanthin-chlorophyll protein. Photosynth Res 135:213–225CrossRefPubMedGoogle Scholar
  42. Khotimchenko SV, Yakovleva IM (2005) Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochemistry 66:73–79CrossRefPubMedGoogle Scholar
  43. Kirchhoff VWJH, Sahai Y, Casiccia CARS, Zamorano BF, Valderrama VV (1997) Observations of the 1995 ozone hole over Punta Arenas, Chile. J Geophys Res 102:16.109–16.120CrossRefGoogle Scholar
  44. Koch K, Thiel M, Tellier F, Hagen W, Graeve M, Tala F, Laeseke P, Bischof K (2015) Species separation within the Lessonia nigrescens complex (Phaeophyceae, Laminariales) is mirrored by ecophysiological traits. Bot Mar 58:81–92Google Scholar
  45. Koch K, Thiel M, Hagen W, Graeve M, Gómez I, Jofre D, Hofmann LC, Tala F, Bischof K (2016) Short- and long-term acclimation patterns of the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) along a depth gradient. J Phycol 52:260–273CrossRefPubMedGoogle Scholar
  46. Kumar M, Kumari P, Gupta V, Reddy CRK, Jha B (2010) Biochemical responses of red alga Gracilaria corticata (Gracilariales, Rhodophyta) to salinity induced oxidative stress. J Exp Mar Biol Ecol 391:27–34CrossRefGoogle Scholar
  47. Kumar M, Kumari P, Reddy CRK, Jha B (2014) Salinity and desiccation induced oxidative stress acclimation in seaweeds. In: Bourgougnon N (ed) Advances in botanical research. Academic Press, London pp, pp 91–123Google Scholar
  48. Kumari P, Bijo AJ, Mantri VA, Reddy CRK, Jha B (2013) Fatty acid profiling of tropical marine macroalgae: an analysis from chemotaxonomic and nutritional perspectives. Phytochemistry 86:44–56CrossRefPubMedGoogle Scholar
  49. Lin SM, Huang R, Ogawa H, Liu LC, Wang YC, Chiou Y (2017) Assessment of germling ability of the introduced marine brown alga, Sargassum horneri, in Northern Taiwan. J Appl Phycol 29:2641–2649CrossRefGoogle Scholar
  50. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol 45:633–662CrossRefGoogle Scholar
  51. Mansilla A, Ávila M, Yokoya NS (2012) Current knowledge on biotechnological interesting seaweeds from the Magellan Region, Chile. Rev Bras Farmacogn 22:760–767CrossRefGoogle Scholar
  52. Mansilla A, Ávila M, Ramírez ME, Rodriguez JP, Rosenfeld S, Jaime O, Marambio J (2013a) Macroalgas marinas bentónicas del submareal somero de la ecorregión subantártica de Magallanes, Chile. An Inst Patagon 41:51–64CrossRefGoogle Scholar
  53. Mansilla A, Rodriguez JP, Souza JMC, Rosenfeld S, Ojeda J, Yokoya NS (2013b) Growth responses to temperature, salinity and nutrient variations, and biomass variation and phenology of Ahnfeltia plicata (Rhodophyta, Ahnfeltiales): a commercially interesting agarophyte from the Magellanic Region, Chile. J Appl Phycol 26:1133–1139CrossRefGoogle Scholar
  54. Mansilla A, Méndez F, Murcia S, Rodríguez JP, Marambio J, Rosenfeld S, Bischof K (2016) Adjustment of pigment composition in Desmarestia (Desmarestiaceae) species along a sub-Antarctic to Antarctic latitudinal gradient. Polar Res 35:29383CrossRefGoogle Scholar
  55. Marambio J, Mendez F, Ocaranza P, Rodriguez JP, Rosenfeld S, Ojeda J, Murcia S, Terrados J, Bischof K, Mansilla A (2017a) Seasonal variations of the photosynthetic activity and pigment concentrations in different reproductive phases of Gigartina skottsbergii (Rhodophyta, Gigartinales) in the Magellan Region, sub-Antarctic Chile. J Appl Phycol 29:721–729CrossRefGoogle Scholar
  56. Marambio J, Rodriguez JP, Mendez F, Ocaranza P, Rosenfeld S, Ojeda J, Rautenberger R, Bischof K, Terrados J, Mansilla A (2017b) Photosynthetic performance and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) along a gradient of depth and seasonality in the ecoregion of Magellan, Chile J Appl Phycol 292575–2585Google Scholar
  57. Marquardt R, Schubert H, Varela DA, Huovinen P, Henríquez L, Buschmann AH (2010) Light acclimation strategies of three commercially important red algal species. Aquaculture 299:140–148CrossRefGoogle Scholar
  58. Méndez F, Tala F, Rautenberger R, Ojeda J, Rosenfeld S, Rodríguez JP, Mansilla A (2017) Morphological and physiological differences between two morphotypes of Durvillaea antarctica (Phaeophyceae) from the sub-Antarctic ecoregion of Magallanes, Chile. J Appl Phycol 29:2557–2565CrossRefGoogle Scholar
  59. Mikami K, Hosokawa M (2013) Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int J Mol Sci 14:13763–13781CrossRefPubMedPubMedCentralGoogle Scholar
  60. Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527–543CrossRefPubMedGoogle Scholar
  61. Morgan-Kiss M, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70:222–252CrossRefPubMedPubMedCentralGoogle Scholar
  62. Moss CW, Lambert MA, Merwin WH (1974) Comparison of rapid methods for analysis of bacterial fatty acids. Appl Microbiol 28:80–85PubMedPubMedCentralGoogle Scholar
  63. Nygárd CA, Dring MJ (2008) Influence of salinity, temperature, dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the Baltic and Irish Seas. Eur J Phycol 43:253–262CrossRefGoogle Scholar
  64. Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernández J, Bozzo C, Navarrete E, Osorio A, Rios A (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem 99:98–104CrossRefGoogle Scholar
  65. Ortiz J, Uquiche E, Robert P, Romero N, Quitral V, Llantén C (2009) Functional and nutritional value of the Chilean seaweeds Codium fragile, Gracilaria chilensis and Macrocystis pyrifera. Eur J Lipid Sci Technol 111:320–327CrossRefGoogle Scholar
  66. Pangestuti R, Siahaan EA, Kim SK (2018) Photoprotective substances derived from marine algae. Mar Drugs 16:399CrossRefPubMedCentralGoogle Scholar
  67. Pellizzari F, Silva MC, Silva EM, Medeiros A, Oliveira MC, Yokoy NS, Pupo D, Rosa LH, Colepicolo P (2017) Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol 40:1671–1685CrossRefGoogle Scholar
  68. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–670Google Scholar
  69. Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237CrossRefGoogle Scholar
  70. Rautenberger R, Bischof K (2016) Dynamic summer solar radiation in Antarctic coastal ecosystems and its effects on photosynthesis of the endemic Antarctic brown macroalga Desmarestia menziesii (Phaeophyceae). Algol Stud 151:123–150CrossRefGoogle Scholar
  71. Rautenberger R, Mansilla A, Gómez I, Wiencke C, Bischof K (2009) Photosynthetic responses to UV-radiation of intertidal macroalgae from the Strait of Magellan (Chile). Rev Chil Hist Nat 82:43–61CrossRefGoogle Scholar
  72. Ríos C, Mutschke E, Montiel A (2010) Estructura de la comunidad macrofaunística bentónica en la boca oriental del estrecho de Magallanes, Chile austral. Ann Inst Patagon 38:83–96Google Scholar
  73. Roach T, Krieger-Liszkay AK (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15:351–362CrossRefPubMedPubMedCentralGoogle Scholar
  74. Rodríguez JP, Terrados J, Rosenfeld S, Méndez F, Ojeda J, Mansilla A (2018) Effects of temperature and salinity on the reproductive phases of Macrocystis pyrifera (L.) C. Agardh (Phaeophyceae) in the Magellan Region. J Appl Phycol.
  75. Rowland FS (2006) Stratospheric ozone depletion. Philos Trans R Soc B 361:769–790CrossRefGoogle Scholar
  76. Sanchez S, Carrasco JF, Fuenzalida H (2012) The Chilean ultraviolet radiation network: monitoring and forecasting UV index for health protection. In: Griffiths J, Rowlands C, Witthaus M (eds) Climate exchange.; searched 8 may 2018
  77. Santos MAZ, Colepicolo P, Pupo D, Fujii MT, Pereira CMP, Mesko MF (2017) Antarctic red macroalgae: a source of polyunsaturated fatty acids. J Appl Phycol 29:759–767CrossRefGoogle Scholar
  78. Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373CrossRefGoogle Scholar
  79. Schmid M, Guihéneuf F, Stengel DB (2014) Fatty acid contents and profiles of 16 macroalgae collected from the Irish coast at two seasons. J Appl Phycol 26:451–463CrossRefGoogle Scholar
  80. Seely GR, Duncan MJ, Vidaver WE (1972) Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar Biol 12:184–188CrossRefGoogle Scholar
  81. Servicio Hidrográfico y Oceanográfico de la Armada de Chile.; searched 8 May 2018
  82. Simioni C, Schmidt EC, Felix MRL, Polo LK, Rover T, Kreusch M, Pereira DT, Chow F, Ramlov F, Maraschin M, Bouzon ZL (2014) Effects of ultraviolet radiation (UVA+UVB) on young gametophytes of Gelidium floridanum: growth rate, photosynthetic pigments, carotenoids, photosynthetic performance, and ultrastructure. Photochem Photobiol 90:1050–1060PubMedGoogle Scholar
  83. Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688CrossRefGoogle Scholar
  84. Skriptsova AV (2016) Seasonal variations in the content of brown algae from Peter the Great Bay, Sea of Japan. Russ J Mar Biol 42:351–356CrossRefGoogle Scholar
  85. Tabakaeva OV, Tabakaev AV (2017) Compositions of lipids and fatty acids from various parts of the brown alga Undaria pinnatifida. Chem Nat Compd 53:843–848CrossRefGoogle Scholar
  86. Tait MA, Hik DS (2003) Is dimethyl sulfoxide a reliable solvent for extracting chlorophyll under field conditions? Photosynth Res 78:87–91CrossRefPubMedGoogle Scholar
  87. Tala F, Penna-Díaz MA, Luna-Jorquera G, Rothäusler E, Thiel M (2017) Daily and seasonal changes of photobiological responses in floating bull kelp Durvillaea antarctica (Chamisso) Hariot (Fucales: Phaeophyceae). Phycologia 56:271–283CrossRefGoogle Scholar
  88. Tang B, Row KH (2013) Development of gas chromatography analysis of fatty acids in marine organisms. J Chromatogr Sci 51:599–607CrossRefPubMedGoogle Scholar
  89. Titlyanov EA, Titlyanova TV, Li X, Hansen GI (2014) Seasonal changes in the intertidal algal communities of Sanya Bay (Hainan Island, China). J Mar Biol Assoc UK 94:879–893CrossRefGoogle Scholar
  90. Varela DA, Hernríquez LA, Fernández PA, Leal P, HernándezGonzález MC, Figueroa FL, Buschmann AH (2018) Photosynthesis and nitrogen uptake of the giant kelp Macrocystis pyrifera (Ochrophyta) grown close to salmon farms. Mar Environ Res 15:93–102CrossRefGoogle Scholar
  91. Vaughan VC, Hassing MR, Lewandowski PA (2013) Marine polyunsaturated fatty acids and cancer therapy. Br J Cancer 108:486–492CrossRefPubMedPubMedCentralGoogle Scholar
  92. Villafañe VE, Helbling EW, Zagarese HE (2001) Solar ultraviolet radiation and its impact on aquatic systems of Patagonia, South America. Ambio 30:112–117CrossRefPubMedGoogle Scholar
  93. White AJ, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 59:63–72CrossRefGoogle Scholar
  94. Wiencke C, Rahmel J, Karsten U, Weykam G, Kirst GO (1993) Photosynthesis of marine macroalgae from Antarctica: light and temperature requirements. Plant Biol 106:77–87Google Scholar
  95. Wong CY, Teoh ML, Phang SM, Lim PE, Beardall J (2015) Interactive effects of temperature and UV radiation on photosynthesis of Chlorella strains from polar, temperate and tropical environments: differential impacts on damage and repair. PLoS One 10:e0139469CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Marco Aurélio Ziemann dos Santos
    • 1
    Email author
  • Samantha Coelho de Freitas
    • 1
  • Lucas Moraes Berneira
    • 1
  • Andres Mansilla
    • 2
  • Maria Soledad Astorga-España
    • 2
  • Pio Colepicolo
    • 3
  • Claudio Martin Pereira de Pereira
    • 1
  1. 1.Center for Chemical, Pharmaceutical and Food SciencesFederal University of PelotasCapão do LeãoBrazil
  2. 2.Laboratory of Antarctic and Sub-Antarctic Marine Ecosystems, University of MagallanesInstituto de Ecología y Biodiversidad (IEB)Punta ArenasChile
  3. 3.Department of Biochemistry, Chemistry InstituteUniversity of São PauloButantãBrazil

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