Advertisement

Journal of Applied Phycology

, Volume 31, Issue 2, pp 835–846 | Cite as

Antioxidant activity of three seaweeds from tropical reefs of Brazil: potential sources for bioprospecting

  • Juliane B. VasconcelosEmail author
  • Edson R. T. P. P. de Vasconcelos
  • Vanessa Urrea-Victoria
  • Patrícia S. Bezerra
  • Thiago N. V. Reis
  • Adilma L. M. Cocentino
  • Daniela M. A. F. Navarro
  • Fungyi Chow
  • Arsenio J. Areces
  • Mutue T. Fujii
VI REDEALGAS WORKSHOP (RIO DE JANEIRO, BRAZIL)

Abstract

We report the first screening for antioxidant activity (AOX) of three dominant seaweeds from low intertidal reefs of Brazil. Sargassum furcatum, Bryothamnion triquetrum, and Osmundaria obtusiloba were extracted with dichloromethane and methanol (2:1), and AOX was measured by five UV-vis microplate spectrophotometric methods: DPPH (2,2-diphenyl-1-picryhydrazyl) and ABTS (2,2-azinobis (3-ethylbenzthiazoline-6-sulfonic acid)) free radical scavenging, metal chelating capacity, total phenolic compounds using reducing power by Folin-Ciocalteu and FRAP (ferric reducing antioxidant power). All studied species showed high AOX, even at very low extract concentrations. We can attribute these results to the stressful environment in which these seaweeds live, high hydrodynamics, air exposure during low spring tides, intense solar radiation, and other factors that may contribute to oxidative stress, featuring O. obtusiloba as a new source of natural antioxidants.

Keywords

Algae Antioxidant assays Oxidative stress Tropical reefs Osmundaria 

Notes

Funding information

This work was partially supported by research grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Proc. 484647/2012-1). The first author thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the doctoral fellowship. MTF and FC thanks CNPq for the productivity fellowship (Proc. 304899/2017-8 and Proc. 303937/2015-7).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abrahamsson K, Choo KS, Pedersén M, Johansson G, Snoeijs P (2003) Effects of temperature on the production of hydrogen peroxide and volatile halocarbons by brackish-water algae. Phytochemistry 64:725–734CrossRefGoogle Scholar
  2. Ahn CB, Kang DS, Shin TS, Jung BM (2004) Free radical scavenging activity of enzymatic extracts from a Brown seaweed Scytosiphon lomentaria by electron spin resonance spectrometry. Food Res Int 37:253–258CrossRefGoogle Scholar
  3. Alencar DB, Silva SR, Pires-Cavalcante K, Lima RL, Pereira Junior FN, Sousa MB, Sampaio AH (2014) Antioxidant potential and cytotoxic activity of two red seaweed species, Amansia multifida and Meristiella echinocarpa, from the coast of Northeastern Brazil. An Acad Bras Ciênc 86:251–263CrossRefGoogle Scholar
  4. Alencar DB, de Carvalho FCT, Rebouças RH, dos Santos DR, dos Santos Pires-Cavalcante KM, de Lima RL, Sampaio AH (2016) Bioactive extracts of red seaweeds Pterocladiella capillacea and Osmundaria obtusiloba (Floridophyceae: Rhodophyta) with antioxidant and bacterial agglutination potential. Asian Pac J of Trop Med 9:372–379Google Scholar
  5. Altuntaş G, Değer Y (2017) The effects of butylated hydroxyl toluene on the total antioxidant status/ total oxidant stress and biochemical parameters in rats. World J Pharm Pharm Sci 6:199–210Google Scholar
  6. Amade P, Lemee R (1998) Chemical defense of the Mediterranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol 43:287–300CrossRefGoogle Scholar
  7. Amaral ACZ, Corte GN, Filho JSR, Denadai MR, Colling LA, Borzone C, Roberto J (2016) Brazilian sandy beaches: characteristics, ecosystem services, impacts, knowledge and priorities. Braz J Oceanogr 64:5–16Google Scholar
  8. Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91Google Scholar
  9. Andreguetti D, Stein EM, Pereira CMP, Pinto E, Colepicolo P (2013) Antioxidant properties and UV absorbance pattern of mycosporine-like amino acids analogs synthesized in an environmentally friendly manner. J Biochem Mol Toxicol 27:305–312CrossRefGoogle Scholar
  10. Aruoma IO (1999) Antioxidant action of plant foods. Use of oxidative DNA damage, as a tool for studying antioxidant efficacy. Free Radic Res 30:419–427CrossRefGoogle Scholar
  11. Bajpai VK (2017) A review on trend of marine sources for the development of functional foods. Indian J Geo Mar Sci 46:1245–252Google Scholar
  12. Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefGoogle Scholar
  13. Bischof K, Gomez I, Molis M, Hanelt D, Karsten U, Lüder U, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166CrossRefGoogle Scholar
  14. Boisvert C, Beaulieu L, Bonnet C, Pelletier E (2015) Assessment of the antioxidant and antibacterial activities of three species of edible seaweeds. J Food Biochem 39:377–387CrossRefGoogle Scholar
  15. Bouzon ZL, Chow F, Zitta CS, dos Santos RW, Ouriques LC, Félix MRL, Osorio LKP, Gouveia C, Martins RP, Latini A, Ramlov F, Maraschin M, Schmidt EC (2012) Effects of natural radiation, photosynthetically active radiation and artificial ultraviolet radiation-B on the chloroplast organization and metabolism of Porphyra acanthophora var. brasiliensis (Rhodophyta, Bangiales). Microsc Microanal 18:1467–1479CrossRefGoogle Scholar
  16. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30CrossRefGoogle Scholar
  17. Cardozo KHM, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AP, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C 146:60–78CrossRefGoogle Scholar
  18. Carreto JI, Carignan MO, Montoya NG (2005) A high resolution reverse-phase liquid chromatography method for the analysis of mycosporine-like amino acids (MAAs) in marine organisms. Mar Biol 146:237–252CrossRefGoogle Scholar
  19. Centella MH, Arévalo-Gallegos A, Parra-Saldivar R, Iqbal HM (2017) Marine-derived bioactive compounds for value-added applications in bio-and non-bio sectors. J Clean Prod 168:1559–1565CrossRefGoogle Scholar
  20. Denton A, Chapman ARO, Markham J (1990) Size-specific concentrations of phlorotannins (antiherbivore compounds) in three species of Fucus. Mar Ecol Prog Ser 65:103–104CrossRefGoogle Scholar
  21. Díaz AC, Espino ML, Arzoz NS, Velurtas SM, Ponce NMA, Stortz CA, Fenucci JL (2017). Free radical scavenging activity of extracts from seaweeds Macrocystis pyrifera and Undaria pinnatifida: applications as functional food in the diet of prawn Artemesia longinaris. Lat Am J Aquat Res 45:104–112Google Scholar
  22. Dinis TCP, Madeira VMC, Almeida LM (1994) Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch Biochem Biophys 315:161–169CrossRefGoogle Scholar
  23. Duh PD (1998) Antioxidant activity of burdock (Arctium lappa Linne): its scavenging effect on free radical and active oxygen. J Am Oil Chem Soc 75:455–461CrossRefGoogle Scholar
  24. Dunlap WC, Yamamoto T (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine–glycine. Comp Biochem Physiol B 112:105–114CrossRefGoogle Scholar
  25. Ferreira ICFR, Baptista P, Vilas-Boas M, Barros L (2007) Free-radical scavenging capacity and reducing power of wild edible mushrooms from northeast Portugal: individual cap and stipe activity. Food Chem 100:1511–1516CrossRefGoogle Scholar
  26. Frankel EN, Meyer AS (2000) The problems of using one-dimensional methods to evaluate multifunctional food and biological antioxidants. J Sci Food Agric 80:1925–1941CrossRefGoogle Scholar
  27. Fujimoto K, Kaneda T (1980) Screening test for antioxigenic compounds from marine algae and fraction from Eisenia bicyclis and Undaria pinnatifida. Bull Jpn Soc Sci Fish 46:1125–1130CrossRefGoogle Scholar
  28. Fujimoto K, Kaneda T (1984) Separation of antioxygenic (antioxidant) compounds from marine algae. Hydrobiologia 116:111–113CrossRefGoogle Scholar
  29. Ganesan P, Chandini SK, Bhaskar N (2008) Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds. Bioresour Technol 99:2717–2723CrossRefGoogle Scholar
  30. Guaratini T, Lopes NP, Marinho-Soriano E, Colepicolo P, Pinto E (2012) Antioxidant activity and chemical composition of the non polar fraction of Gracilaria domingensis (Kützing) Sonder ex Dickie and Gracilaria birdiae (Plastino & Oliveira). Braz J Pharmacog 22:724–729CrossRefGoogle Scholar
  31. Harb TB, Torres PB, Pires JS, Dos Santos DYAC, Chow F (2016) Ensaio em microplaca do potencial antioxidante através do sistema quelante de metais para extratos de algas. Instituto de Biociências, Universidade de São PauloGoogle Scholar
  32. Höhn A, Weber D, Jung T, Ott C, Hugo M, Kochlik B, Kehm R, König J, Grune T, Castro JP (2017) Happily (n)ever after: aging in the context of oxidative stress, proteostasis loss and cellular senescence. Redox Biol 11:482–501CrossRefGoogle Scholar
  33. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  34. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856CrossRefGoogle Scholar
  35. Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Mar Biol 101:115–119CrossRefGoogle Scholar
  36. Ito N, Hirose M, Fukushima S, Tsuda H, Shirai T, Tatematsu M (1986) Studies on antioxidants: their carcinogenic and modifying effects on chemical carcinogenesis. Food Chem Toxicol 24:1071–1082CrossRefGoogle Scholar
  37. Jacobsen C, Sørensen ADM (2015) The use of antioxidants in the preservation of food emulsion systems. In: Shahidi F (ed) Handbook of antioxidants for food preservation. Elsevier, Amsterdam, pp 389–412CrossRefGoogle Scholar
  38. Karsten U (2008) Defense strategies of algae and cyanobacteria against solar ultraviolet radiation. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 273–296CrossRefGoogle Scholar
  39. Kelman D, Posner EK, McDermid KJ, Tabandera NK, Wright PR, Wright AD (2012) Antioxidant activity of Hawaiian marine algae. Mar Drugs 10:403–416CrossRefGoogle Scholar
  40. Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and method for their quantification. Toxicol Pathol 30:620–650CrossRefGoogle Scholar
  41. Kuda T, Tsunekawa M, Goto H, Araki Y (2005) Antioxidant properties of four edible algae harvested in the Noto Peninsula. Japan. J Food Compos Anal 18:625–633CrossRefGoogle Scholar
  42. Kumaran A, Karunakaran RJ (2007) In vitro antioxidant properties of methanol extracts of five Phillanthus species from India. LWT Food Sci Technol 40:344–352CrossRefGoogle Scholar
  43. Laganà P, Avventuroso E, Romano G, Gioffré ME, Patanè P, Parisi S, Moscato S, Delia S (2017) Classification and technological purposes of food additives: The European point of view. In: Parisi S (ed) Chemistry and hygiene of food additives. Springer, Cham, pp 1–21CrossRefGoogle Scholar
  44. Lahaye M (2001) Chemistry and physico-chemistry of phycocolloids. Cah Biol Mar 42:137–157Google Scholar
  45. Le Lann K, Rumin J, Cérantola S, Culioli G, Stiger-Pouvreau V (2013) Spatiotemporal variations of diterpene production in the brown macroalga Bifurcaria bifurcata from the western coasts of Brittany (France). J Appl Phycol 26:1207–1214CrossRefGoogle Scholar
  46. Le Tutour B, Benslimane F, Gouleau MP, Gouygou JP, Saldan B, Quemeneur F (1990) Antioxidative activities of algae extracts, synergistic effect with vitamin E. Phytochem 29:3759–3765CrossRefGoogle Scholar
  47. Li Z, Wang B, Zhang Q, Qu Y, Xu H, Li G (2012) Preparation and antioxidant property of extract and semipurified fractions of Caulerpa racemosa. J Appl Phycol 24:1527–1536CrossRefGoogle Scholar
  48. Maréchal JP, Culioli G, Hellio C, Thomas-Guyon H, Callow ME, Clare AS, Ortalo-Mané A (2004) Seasonal variation in antifouling activity of crude extracts of the brown alga Bifurcaria bifurcata (Cystoseiraceae) against cyprids of Balanus amphitrite and the marine bacteria Cobetia marina and Pseudoalteromonas haloplanktis. J Exp Mar Biol Ecol 313:47–62CrossRefGoogle Scholar
  49. Martins CDL, Ramlov F, Carneiro NPN, Gestinari LM, Santos BF, Bento LM, Lhullier C, Gouvea L, Bastos E, Horta PA, Soares AR (2012) Antioxidant properties and total phenolic contents of some tropical seaweeds of the Brazilian coast. J Appl Phycol 25:1179–1187CrossRefGoogle Scholar
  50. Maschek JA, Baker BA (2008) The chemistry of algal secondary metabolism. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 1–22Google Scholar
  51. Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH (2008) Antioxidant activities and phenolics content of eight species of seaweed from north Borneo. J Appl Phycol 20:367–373CrossRefGoogle Scholar
  52. Matsukawa R, Dubinsky Z, Kishimoto E, Masaki Z, Masuda Y, Takeuchi T, Chihaara M, Yamamoto Y, Niki E, Karube I (1997) A comparison of screening methods for antioxidant activity in seaweeds. J Appl Phycol 9:29–35CrossRefGoogle Scholar
  53. McKenzie R, Connor B, Bodeker G (1999) Increased summertime UV radiation in New Zealand in response to ozone loss. Science 285:1709–1711CrossRefGoogle Scholar
  54. Murphy TM (1983) Membranes as targets of ultraviolet radiation. Physiol Plant 58:381–388CrossRefGoogle Scholar
  55. Nakagawa Y, Yaguchi K, Suzuki T (1994) Comparative cytotoxicity between butylated hydroxytoluene and its methylcarbamate derivative, terbucarb, on isolated rat hepatocytes. Bull Environ Contam Toxicol 52:511–515CrossRefGoogle Scholar
  56. Nakamura H, Kobayashi J, Hirata Y (1982) Separation of mycosporine-like amino acids in marine organisms using reversed-phase high-performance liquid chromatography. J Chromatogr A 250:113–118CrossRefGoogle Scholar
  57. Ngo DH, Vo TS, Ngo DN, Wijesekara I, Kim SK (2012) Biological activities and potential health benefits of bioactive peptides derived from marine organisms. Int J Biol Macromol 51:378–383CrossRefGoogle Scholar
  58. Novoa AV, Motidome M, Mancini-Filho J, Linares AF, Tanae MM, Torres LMB, Lapa AJ (2001) Actividad antioxidant y ácidos fenólicos del alga marina Bryothamnion triquetrum (SG Gmelim) Howe. Braz J Pharm Sci 37:373–382Google Scholar
  59. Novoa AV, Andrade-Wartha ERS, Linares AF, Silva AMO, Genovese MI, González AEB, Vuorela P, Costa A, Mancini-Filho J (2011) Antioxidant activity and possible bioactive components in hydrophilic and lipophilic fractions from the seaweed Halimeda incrassata. Braz J Pharmacog 21:53–57CrossRefGoogle Scholar
  60. O’Sullivan AM, O’Callaghan YC, O'Grady MN, Queguineur B, Hanniffy D, Troy DJ, Kerry JP, O’Brien NM (2011) In vitro and cellular antioxidant activities of seaweed extracts prepared from five brown seaweeds harvested in spring from the west coast of Ireland. Food Chem 126:1064–1070CrossRefGoogle Scholar
  61. Olson JA (1999) Carotenoids and human health. Arch Latinoam Nutr 49:7–11Google Scholar
  62. Paloczi J, Varga ZV, Hasko G, Pacher P (2018) Neuroprotection in oxidative stress-related neurodegenerative diseases: role of endocannabinoid system modulation. Antioxid Redox Signal 29:75–108CrossRefGoogle Scholar
  63. Paul VJ, Puglisi MP (2004) Chemical mediation of interactions among marine organisms. Nat Prod Rep 21:189–209CrossRefGoogle Scholar
  64. Pavia H, Toth GB (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225CrossRefGoogle Scholar
  65. Pavia H, Cervin G, Lindgren A, Aberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139–146CrossRefGoogle Scholar
  66. Pedersen A (1984) Studies on phenol content and heavy metal uptake in fucoids. Hydrobiologia 116:498–504CrossRefGoogle Scholar
  67. Pires KMS, Alencar DB, Sousa MB, Sampaio AH, Saker-Sampaio S (2008) Teores de α- e β-caroteno em macroalgas marinhas desidratadas. Rev Ciênc Agron 39:257–262Google Scholar
  68. Pires J, Torres PB, Santos DYAC, Chow F (2017a) Ensaio em microplaca do potencial antioxidante através do método de sequestro do radical livre DPPH para extratos de algas. Instituto de Biociências, Universidade de São PauloGoogle Scholar
  69. Pires J, Torres PB, Santos DYAC, Chow F (2017b) Ensaio em microplaca de substâncias redutoras pelo método do Folin-Ciocalteu para extratos de algas. Instituto de Biociências, Universidade de São PauloGoogle Scholar
  70. Pires-Cavalcanti KMS, Alencar DB, Sousa MB, Sampaio AH, Saker-Sampaio S (2011) Seasonal changes of α-tocopherol in green marine algae (Caulerpa genus). J Food Sci 76:775–781CrossRefGoogle Scholar
  71. Poprac P, Jomova K, Simunkova M, Kollar V, Christopher J, Valko RM (2017) Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci 38:592–607CrossRefGoogle Scholar
  72. Porse H, Rudolph B (2017) The seaweed hydrocolloid industry: 2016 updates, requirements, and outlook. J Appl Phycol 29:2187–2200CrossRefGoogle Scholar
  73. Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round FE, Chapman DJ (eds) Progress in phycological research. Biopress Ltd., Bristol, pp 129–241Google Scholar
  74. Ragan MA, Jensen A (1978) Quantitative studies on brown algal phenols. II. Seasonal variation in polyphenol content of Ascophyllum nodosum (L.) Le Jol. and Fucus vesiculosus (L.). J Exp Mar Biol Ecol 34:245–258CrossRefGoogle Scholar
  75. Reaven PD, Witzum JL (1996) Oxidised LDL in atherogenesis. Role of dietary modification. Annu Rev Nutr 16:51–71CrossRefGoogle Scholar
  76. Rioux LE, Turgeon SL (2015) Seaweed carbohydrates. In: Tiwari BK, Troy DJ (eds) Seaweed sustainability. Elsevier, Amsterdam, pp 141–192CrossRefGoogle Scholar
  77. Rocha FD, Pereira RC, Kaplan MAC, Teixeira VL (2007) Produtos naturais de algas marinhas e seu potencial antioxidante. Braz J Pharmacogn 17:631–639CrossRefGoogle Scholar
  78. Rodrıguez-Delgado MA, Malovana S, Perez JP, Borges T, Garcıa Montelongo FJ (2001) Separation of phenolic compounds by high-performance liquid chromatography with absorbance and fluorimetric detection. J Chromatogr A 912:249–257CrossRefGoogle Scholar
  79. Rufino MSM, Alves RE, Brito ES, Morais SM, Sampaio CG, Pérez-Jimeénez J, Sura-Calixto FD (2007) Metodologia científica: determinação da atividade antioxidante total em frutas pela captura do radical livre DPPH. Comunicado Técnico 127Google Scholar
  80. Schmidt EC, Marthiellen RDL, Polo LK, Kreusch MG, Pereira DT, Costa GB, Simioni C, Martins RP, Latini A, Chow F, Ramlov F, Pereira A, Maraschin M, Ouriques LC, Steiner N, Bouzon ZL (2015) Influence of cadmium and salinity in the red alga Pterocladiella capillacea: cell morphology, photosynthetic performance and antioxidant systems. Braz J Bot 38:737–749CrossRefGoogle Scholar
  81. Shoaf WT, Lium BW (1976) Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnol Oceanogr 21:926–928CrossRefGoogle Scholar
  82. Silva AMOE, Vidal-Novoa A, Gonzalez AEB, Pinto JR, Mancini DAP, Reina-Urquijo WY, Mancini-Filho J (2012) In vivo and in vitro antioxidant activity and hepatoprotective properties of polyphenols from Halimeda opuntia (Linnaeus) Lamoroux. Redox Rep 17:47–53CrossRefGoogle Scholar
  83. Singleton V, Rossi J (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  84. Sinha RP, Klisch M, Gröniger A, Häder DP (2000) Mycosporine-like amino acids in the marine red alga Gracilaria cornea—effects of UV and heat. Environ Exp Bot 43:33–43CrossRefGoogle Scholar
  85. Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16:245–262CrossRefGoogle Scholar
  86. Smith RE, Tran K, Richards KM (2014) Bioactive annonaceous acetogenins. Stud Nat Prod Chem 41:95–117CrossRefGoogle Scholar
  87. Sousa MB, Pires KMS, Alencar DB, Sampaio AH, Saker-Sampaio S (2008) α-, β-caroteno e α-tocoferol em algas marinhas in natura. Cienc Tecnol Aliment 28:953–958CrossRefGoogle Scholar
  88. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson MAX, Martin KD (2007). Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57:573–583Google Scholar
  89. Steghens JP, van Kappelb AL, Ribolib E, Collombel C (1997) Simultaneous measurement of seven carotenoids, retinol and α-tocopherol in serum by high-performance liquid chromatography. J Chromatogr B 694:71–81CrossRefGoogle Scholar
  90. Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205CrossRefGoogle Scholar
  91. Targett NM, Boettcher AA, Targett TE, Vrolijk NH (1995) Tropical marine herbivore assimilation of phenolic-rich plants. Oecologia 103:170–179CrossRefGoogle Scholar
  92. Thomas NV, Kim SK (2011) Potential pharmacological applications of polyphenolic derivates from marine brown algae. Environ Toxicol Pharmacol 32:325–335CrossRefGoogle Scholar
  93. Tierney MS, Smyth TJ, Hayes M, Soler-Vila A, Croft AK, Brunton N (2013) Influence of pressurised liquid extraction and solid–liquid extraction methods on the phenolic content and antioxidant activities of Irish macroalgae. Int J Food Sci Technol 48:860–869CrossRefGoogle Scholar
  94. Torres PB, Chow F, Ferreira MJ, dos Santos DYAC (2016) Mycosporine-like amino acids from Gracilariopsis tenuifrons (Gracilariales, Rhodophyta) and its variation under high light. J Appl Phycol 28:2035–2040CrossRefGoogle Scholar
  95. Torres PB, Pires J, dos Santos DYAC, Chow F (2017) Ensaio do potencial antioxidante de extratos de algas através do sequestro do ABTS•+ em microplaca. Instituto de Biociências, Universidade de São PauloGoogle Scholar
  96. Urrea-Victoria V, Pires J, Torres PB, dos Santos DYAC, Chow F (2016) Ensaio antioxidante em microplaca do poder de redução do ferro (FRAP) para extratos de algas. Instituto de Biociências, Universidade de São PauloGoogle Scholar
  97. Van Alstyne KL, Whitman SL, Ehlig JM (2001) Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Mar Biol 139:201–210CrossRefGoogle Scholar
  98. Vass I (1997) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of photosynthesis. Marcel Dekker Inc., New York, pp 931–949Google Scholar
  99. Vinayak RC, Sabu SA, Chatterji A (2011) Bio-prospecting of a few brown seaweeds for their cytotoxic and antioxidant activities. Evid Based Complement Alternat Med 5:1–9CrossRefGoogle Scholar
  100. von Elbe JH, Schwartz SJ (1996) Colorants. In: Owen R, Fennema E (eds) Food Chemistry. Dekker Inc., New York, pp 685–691Google Scholar
  101. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific Publications, Oxford, pp 83–85Google Scholar
  102. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982CrossRefGoogle Scholar
  103. Wijesinghe WA, Jeon YJ (2012) Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia 83:6–12CrossRefGoogle Scholar
  104. Yuan YV, Westcott ND, Hu C, Kitts DD (2009) Mycosporine-like amino acid composition of the edible red alga, Palmaria palmata (dulse) harvested from the west and east coasts of Grand Manan Island, New Brunswick. Food Chem 112:321–328CrossRefGoogle Scholar
  105. Zhang Y, Unnikrishnan A, Deepa SS, Liu Y, Li Y, Ikeno Y, Sosnowska D, Remmen HV, Richardson A (2017) A new role for oxidative stress in aging: the accelerated aging phenotype in mice is correlated to increased cellular senescence. Redox Biol 11:30–37CrossRefGoogle Scholar
  106. Zubia M, Robledo DY, Freile-Pelegrin Y (2007) Antioxidant activities in tropical marine macroalgae from the Yucatan Peninsula, Mexico. J Appl Phycol 19:449–458CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Juliane B. Vasconcelos
    • 1
    Email author
  • Edson R. T. P. P. de Vasconcelos
    • 1
  • Vanessa Urrea-Victoria
    • 2
  • Patrícia S. Bezerra
    • 3
  • Thiago N. V. Reis
    • 1
  • Adilma L. M. Cocentino
    • 1
  • Daniela M. A. F. Navarro
    • 3
  • Fungyi Chow
    • 2
  • Arsenio J. Areces
    • 4
  • Mutue T. Fujii
    • 5
  1. 1.Laboratório de Macroalgas, Departamento de OceanografiaUniversidade Federal de PernambucoRecifeBrazil
  2. 2.Laboratório de Algas Marinhas “Édison José de Paula”, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  3. 3.Laboratório de Ecologia Química, Departamento de Química FundamentalUniversidade Federal de PernambucoRecifeBrazil
  4. 4.Instituto de Geografia TropicalHavanaCuba
  5. 5.Núcleo de Pesquisa em FicologiaInstituto de BotânicaSão PauloBrazil

Personalised recommendations