Differential photosynthetic, phytochemical and antioxidative responses of three macroalgae Ulva lactuca, Gracilaria salicornia and Turbinaria ornata exposed to thermal and irradiance conditions




Abstract. Narrain D, Baulroop J, Bhagooli R, Bahorun T. 2023. Differential photosynthetic, phytochemical and antioxidative responses of three macroalgae Ulva lactuca, Gracilaria salicornia and Turbinaria ornata exposed to thermal and irradiance conditions. Indo Pac J Ocean Life 7: 1-15. Worldwide climate change leads to a varied distribution of aquatic organisms due to their differences in susceptibility to environmental conditions. Being at the base of marine food webs, macroalgae are potential candidates to investigate the effects of changing environmental conditions and to study the adaptation mechanisms. This study examined the effects of in vitro thermal and irradiance conditions (Control - CLCT: 1.55±0.63 µmol quanta m-2s-1 and 28°C; Control light and high temperature - CLHT: 1.55±0.63 µmol quanta m-2s-1 and 32°C; Moderate light and control temperature – MLCT: 100±63.6 µmol quanta m-2s-1 and 28°C; Moderate light and high temperature – MLHT: 100±63.6 µmol quanta m-2s-1 and 32°C) for 1 week on the photosynthetic performance, phytochemical contents, and antioxidant potential of three macroalgae Ulva lactuca L., Gracilaria salicornia (C.Agardh) E.Y.Dawson and Turbinaria ornata (Turner) J.Agardh found in the lagoons of Mauritius Island. Our results indicate variable responses of the three test macroalgal species when exposed to combinations of temperature and light conditions. Differential responses were found to be both species- and stress-specific. Chlorophyll fluorescence measurements using a Diving Pulse-Amplitude Modulated (D-PAM) fluorometer indicated a significant increase (p<0.001) in relative maximum electron transport rate (rETRmax) of U. lactuca in all stress treatments implying higher photosynthetic activity compared to control conditions. A significant decrease (p<0.001) in rETRmax of G. salicornia under MLHT and the collapse of photosystem II (PSII) activity (Fv/Fm) in T. ornata, along with both species exhibiting visual pigment degradation, are suggestive of chronic photo-inhibition in these two macroalgal species. Antioxidant activities (FRAP and TEAC assays) correlated stronger to flavonoid contents (FRAP, r=0.909; TEAC, r=0.845) than to phenol contents (FRAP, r=0.688; TEAC, r=0.758). An increase in temperature and irradiance severely damaged the PSII of T. ornata and G. salicornia, while U. lactuca could photo-physiologically adjust to changing environmental conditions, showing its robustness. The elevated temperature significantly affected the photosynthetic performance and antioxidative activities of the tested macroalgal species (p<0.001). These findings are discussed to possible influence on defense mechanisms of these macroalgal species and their aquaculture potential in an era of climate change. Further research using field-based manipulations as well as molecular analysis is warranted to thoroughly understand the potential mechanisms involved in variable responses of these tested macroalgae.



Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C. 2002. Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord II. Pigment accumulation and accumulation and biochemical defense systems against high light stress. Mar Biol 140 (6): 1087-1095. DOI: 10.1007/s00227-002-0792-y.
Asimakis E, Shehata AA, Eisenreich W, Acheuk F, Lasram S, Basiouni S, Emekci M, Ntougias S, Taner G, May-Simera H, Yilmaz M, Tsiamis G. 2022. Algae and their metabolites as potential bio-pesticides. Microorganisms 10 (2): 307. DOI: 10.3390/microorganisms10020307.
Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8 (7): 343-351. DOI: 10.1016/S1360-1385(03)00136-5.
Bahorun T, Luximon?Ramma A, Crozier A, Aruoma OI. 2004. Total phenol, flavonoid, proanthocyanidin and vitamin C levels and antioxidant activities of Mauritian vegetables. J Sci Food Agric 84 (12): 1553-1561. DOI: 10.1002/jsfa.1820.
Barbosa M, Valentão P, Andrade PB. 2014. Bioactive compounds from macroalgae in the new millennium: Implications for neurodegenerative diseases. Mar drugs 12 (9): 4934-4972. DOI: 10.3390/md12094934.
Beetul K, Gopeechund A, Kaullysing D, Mattan-Moorgawa S, Puchooa D, Bhagooli R. 2016. Challenges and opportunities in the present era of marine algal applications. In: Dhanasekaran D (eds). Algae - Organisms for Imminent Biotechnology. InTech Open, London. DOI: 10.5772/63272.
Benzie IF, Strain JJ. 1996. The FRAP of plasma as a measure of antioxidant power: The FRAP assay. J Anal Biochem 239: 219-224. DOI: 10.1006/abio.1996.0292.
Bhagooli R, Baird AH, Ralph P. 2008. Coral host protects its photosynthetic symbionts from thermal and light stresses. Proceedings of the 11th International Coral Reef Symposium 2008, Fort Lauderdale, Florida, USA.
Bhagooli R, Kaullysing D. 2019. Seas of Mauritius-Chapter 12. In: Sheppard CCR (eds). World Seas: An Environmental Evaluation, 2nd Edition, Volume II: The Indian Ocean to the Pacific. Elsevier, Amsterdam. DOI: 10.1016/B978-0-08-100853-9.00016-6.
Bhagooli R, Mattan-Moorgawa S, Kaullysing D, Chumun PK, Klaus R, Munbodhe V. 2021c. Status and sustainability of reefs and shorelines of the Republic of Mauritius. In Gunputh RP (eds). Sustainable Development Goals. Star Publications Pvt. Ltd., New Delhi, India.
Bhagooli R, Mattan-Moorgawa S, Kaullysing D, Louis YD, Gopeechund A, Ramah S, Soondur M, Pilly SS, Beesoo R, Wijayawanti DP, Bachok ZB, Monrás VC, Casareto BE, Suzuki Y, Baker AC. 2021a. Chlorophyll fluorescence - a tool to assess photosynthetic performance and stress photo-physiology in symbiotic marine invertebrates and seaplants. Mar Pollut Bull 165: 112059. DOI: 10.1016/j.marpolbul.2021.112059.
Bhagooli R, Ramah S, Kaullysing D, Gopeechund A, Bergstad OA. 2021b. First field observations of Halimeda beds at depths of 37-62 m at Saya de Malha and Nazareth banks, Mascarene Plateau, Western Indian Ocean. Special Issues 2/2021 – Studies on the Mascarene Plateau. West Indian Ocean J Mar Sci 2: 183-187. DOI: 10.4314/wiojms.si2021.2.14.
Bhagooli R, Soondur M, Ramah S, Gopeechund A, Kaullysing D. 2021d. A first study on the variable photo-physiological performance of macroalgae and seagrasses from Saya de Malha and Nazareth Banks, Mascarene Plateau. Special Issues 2/2021-Studies on the Mascarene Plateau. West Indian Ocean J Mar Sci 95-108. DOI: 10.4314/wiojms.si2021.2.7.
Bhagooli R, Taleb-Hossenkhan N. 2012. Thermal spatial heterogeneity and coral bleaching: implications for habitat refuges. In Proceedings of the 12th International Coral Reef Symposium Cairns, Australia, 9D.
Bolton JJ, Bhagooli R, Mattio L. 2012. The Mauritian seaweed flora: diversity and potential for sustainable utilization. Univ Mauritius Res J 18: 6-17.
Brown BE. 1997. Coral bleaching: Causes and consequences. Coral Reefs 16: 129-138. DOI: 10.1007/s003380050249.
Buchel C, Wilhelm C. 1993. In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems and perspectives. Photochem Photobiol 58: 137-148. DOI: 10.1111/j.1751-1097.1993.tb04915.x.
Campos A, Lissi E. 1996. Kinetics of the reaction between ABTS derived radical cations and phenols. Intl J Chem Kinet 29: 219-224. DOI: 10.1002/(SICI)1097-4601(1997)29:3<219::AID-KIN9>3.0.CO;2-X.
Cardozo KH, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E. 2007. Metabolites from algae with economical impact. Comp. Biochem. Physiol C: Toxicol Pharmacol 146 (1): 60-78. DOI: /10.1016/j.cbpc.2006.05.007.
Carvalho AM, Neto AM, Tonon AP, Pinto E, Cardozo KH, Brigagao MR, Barros MP, Torres MA, Magalhães P, Campos SC, Guaratini T. 2004. Circadian protection against oxidative stress in marine algae. Hypnos 1 (Supplementary 1): 142-157.
Chow WS, Hope AB, Anderson JM. 1989. Oxygen per flash from leaf disks quantifies photosystem II. Biochimica et Biophysica Acta 973: 105-108. DOI: 10.1016/S0005-2728(89)80408-6.
Colvard N, Helmuth B. 2016. Nutrients influence the thermal ecophysiology of an intertidal macroalga: Multiple stressors or multiple drivers? Ecol Appl 2: 669-681. DOI: DOI: 10.1002/eap.1475.
Cronin G, Hay ME. 1996. Within-plant variation in seaweed palatability and chemical defenses: Optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 105 (3): 361-368. DOI: 10.1007/BF00328739.
Davidson IR. 1991. Environmental effects on algal photosynthesis: Temperature. J Phycol 27 (1): 2-8. DOI: 10.1111/j.0022-3646.1991.00002.x.
De Clerck O, Bolton JJ, Anderson RJ, Coppejans E. 2005. Guide to the seaweeds of KwaZulu-Natal. Scripta Botanica Belgica 33: 1-294.
Eismann AI, Reis RP, da Silva AF, Cavalcanti DN. 2020. Ulva spp. carotenoids: Responses to environmental conditions. Algal Res 48: 101916. DOI: 10.1016/j.algal.2020.101916.
Feder ME, Hofmann GE. 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Ann Rev Physiol 61: 243-282. DOI: 10.1146/annurev.physiol.61.1.243.
Foyer CH, Shigeoka S. 2011. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155: 93-100. DOI: 10.1104/pp.110.166181.
Fulton CJ, Berkström C, Wilson SK, Abesamis RA, Bradley M, Åkerlund C, Barrett LT, Bucol AA, Chacin DH, Chong?Seng KM, Coker DJ. 2020. Macroalgal meadow habitats support fish and fisheries in diverse tropical seascapes. Fish Fish 21 (4): 700-717. DOI: 10.1111/faf.12455.
Gao K, Beardall J. 2022. Using macroalgae to address UN Sustainable Development goals through CO2 remediation and improvement of the aquaculture environment. Appl Phycol 2022: 1-8. DOI: 10.1080/26388081.2022.2025617.
Gao Z, Xu D, Meng C, Zhang X, Wang Y, Li D, Zou J, Zhuang Z, Ye N. 2014. The green tide-forming macroalga Ulva linza outcompetes the red macroalga Gracilaria lemaneiformis via allelopathy and fast nutrients uptake. Aquat Ecol 48 (1): 53-62. DOI: 10.1007/s10452-013-9465-9.
Geertz-Hansen O, Sand-Jensen K. 1992. Growth rates and photon yield of growth in natural populations of a marine macroalga Ulva lactuca. Mar Ecol Prog Ser 81: 179-183. DOI: 10.3354/meps081179.
Genty B, Briantais JM, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92. DOI: 10.1016/S0304-4165(89)80016-9.
Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48 (12): 909-930. DOI: 10.1016/j.plaphy.2010.08.016.
Gopeechund A, Bhagooli R, Neergheen VS, Bolton JJ, Bahorun T. 2020. Anticancer activities of marine macroalgae: Status and future perspectives. In Biodiversity and Biomedicine. Academic Press, Cambridge. DOI: 10.1016/B978-0-12-819541-3.00014-1.
Guiry MD, Guiry GM. 2017. AlgaeBase. World-Wide Electronic Publication, National University of Ireland, Galway.
Gutteridge JM, Halliwell B. 1990. The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci 15 (4): 129-135. DOI: 10.1016/0968-0004(90)90206-q.
Häder DP, Lebert M, Sinha RP, Barbieri ES, Helbling EW. 2002. Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochem Photobiol Sci 1 (10): 809-814. DOI: 10.1039/b206152j.
Hanelt D. 1998. Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Mar Biol 131: 361-369. DOI: 10.1007/s002270050329.
Harley CD, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH. 2012. Effects of climate change on global seaweed communities. J Phycol 48 (5): 1064-1078. DOI: 10.1111/j.1529-8817.2012.01224.x.
Hofmann GE, Todgham AE. 2010. Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Ann Rev Physiol 72: 127-145. DOI: 10.1146/annurev-physiol-021909-135900.
Ishikawa T, Shigeoka S. 2008. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72: 1143-1154. DOI: 10.1271/bbb.80062.
Jagtap TG. 1993. Studies on littoral and sublittoral macrophytes around the Mauritius coast. Atoll Res Bull 382: 1-10. DOI: 10.5479/si.00775630.382.1.
Jahns P, Holzwarth AR. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta-Bioenergetics 1817 (1): 182-193. DOI: 10.1016/j.bbabio.2011.04.012.
Ji Y, Gao K. 2021. Effects of climate change factors on marine macroalgae: A review. Adv Mar Biol 88: 91-136. DOI: 10.1016/bs.amb.2020.11.001.
Kakinuma M, Shibahara N, Ikeda H, Maegawa M, Amano H. 2001. Thermal stress responses of a sterile mutant of Ulva pertusa (Chlorophyta). Fish Sci 67: 287-294. DOI: 10.1046/j.1444-2906.2001.00229.x.
Kalasariya HS, Pereira L. Patel NB. 2022. Pioneering role of marine macroalgae in cosmeceuticals. Phycology 2: 172-203. DOI: 10.3390/phycology2010010.
Kaullysing D, Gopeechund A, Mattan-Moorgawa S, Taleb-Hossenkhan N, Kulkarni B, Bhagooli R. 2016 Increased density of the corallivore Drupella cornus on Acropora muricata colonies overgrown by Padina boryana. In proceedings of the 13th International Coral Reef Symposium, Honolulu, Hawaii.
Kelman D, Posner EK, McDermid KJ, Tabandera NK, Wright PR, Wright AD. 2012. Antioxidant activity of Hawaiian marine algae. Mar Drugs 10 (2): 403-416. DOI: 10.3390/md10020403.
Kumar A, Singh RP, Kumar I, Yadav P, Singh SK, Kaushalendra, Singh PK, Gupta RK, Singh SM, Kesawat MS, Saratale GD, Chung S-M, Kumar M. 2022. Algal metabolites can be an immune booster against COVID-19 pandemic. Antioxidants 11 (3): 452. DOI: 10.3390/antiox11030452.
Lamaison JLC, Carnet A. 1991. Teneurs en principaux flavonoids des fleurs de Crataegeus monogyna (Jacq) et de Crataegeus Iaevigata (Poiret D.C) en fonction de la vegetation. Pharmaceutica Acta Helvetiae 65: 315-320.
Lambrev PH, Miloslavina Y, Jahns P, Holzwarth AR. 2012. On the relationship between non-photochemical quenching and photoprotection of photosystem II. BBA-Bioenergetics 1817 (5): 760-769. DOI: 10.1016/j.bbabio.2012.02.002.
Lesser MP. 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Ann Rev Physiol 68: 253-278. DOI: 10.1146/annurev.physiol.68.040104.110001.
Li G, Qin Z, Zhang J, Lin Q, Ni G, Tan Y, Zou D. 2020. Algal density mediates the photosynthetic responses of a marine macroalga Ulva conglobata (Chlorophyta) to temperature and pH changes. Algal Res 46: 101797.
Li MH, Cherubini P, Dobbertin M, Arend M, Xiao WF, Rigling A. 2013. Responses of leaf nitrogen and mobile carbohydrates in different Quercus species/provenances to moderate climate changes. Plant Biol (Supplementary 1): 177-184. DOI: 10.1111/j.1438-8677.2012.00579.x.
Lindquist S. 1986. The heat-shock response. Ann Rev Biochem 55: 1151-1159. DOI: 10.1146/annurev.bi.55.070186.005443.
Louis YD, Kaullysing D, Gopeechund A, Mattan-Moorgawa S, Bahorun T, Dyall SD, Bhagooli R. 2016. In hospite Symbiodinium photophysiology and antioxidant responses in Acropora muricata on a coast-reef scale: Implications for variable bleaching patterns. Symbiosis 68: 61-72. DOI: 10.1007/s13199-016-0380-4.
Lutchmanen C, Bhagooli R. 2015. An evaluation of public perception of potential sustainable seaweed industry in Mauritius. Proceedings of the ADDGASAT Conference on Science, Technology, Gender and Sustainable Development, Challenges and Opportunities 2025: Legacy for Future Generations 130-142.
Machalek KM, Davison IR, Falkowski PG. 1996. Thermal acclimation and photoacclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19 (9): 1005-1016. DOI: 10.1111/j.1365-3040.1996.tb00207.x.
Maharana D, Das PB, Verlecar XN, Pise NM, Gauns M. 2015. Oxidative stress tolerance in intertidal red seaweed Hypnea musciformis (Wulfen) in relation to environmental components. Environ Sci Pollut Res 22 (23): 18741-18749. DOI: 10.1007/s11356-015-4985-6.
Mattan-Moorgawa S, Bhagooli R, Rughooputh SD. 2012. Thermal stress physiology and mortality responses in scleractinian corals of Mauritius. In Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia.
Mattio L, Zubia M, Loveday B, Crochelet E, Duong N, Payri CE, Bhagooli R, Bolton JJ. 2013. Sargassum (Fucales, Phaeophyceae) in Mauritius and Réunion, western Indian Ocean: Taxonomic revision and biogeography using hydrodynamic dispersal models. Phycologia 52 (6): 578-594. DOI: 10.2216/13-150.1.
Mauritius Research and Innovation Council. 2013. Annual Report, pp 28. Available from: https://www.mric.mu/_files/ugd/d4e70d_ea91a19173504bf29abc0abb4f772997.pdf [Ahttp://www.mrc.org.mu/English/Documents/Annual%20Report%202013.pdf. Accessed on: 28 March 2022].
McMinn A, Ashworth C, Bhagooli R, Martin A, Salleh S, Ralph P, Ryan K. 2012. Antarctic coastal microalgal primary production and photosynthesis. Mar Biol 159 (12): 2827-2837. DOI: 10.1007/s00227-012-2044-0.
Meethoo A, Badal R, Bhagooli R. 2017. Coastal marine activities and coral cover at three tropical coral reefs around an oceanic island, Mauritius. J Mar Sci Res Technol 1-11.
Moreira A, Cruz S, Marques R, Cartaxana P. 2021. The underexplored potential of green macroalgae in aquaculture. Rev Aquac 14: 5-26. DOI: 10.1111/raq.12580.
Moustakas M. 2021. Plant photochemistry, reactive oxygen species, and photoprotection. Photochemistry 2 (1): 5-8. DOI: 10.3390/photochem2010002.
Msuya FE, Buriyo A, Omar I, Pascal B, Narrain K, Ravina JJ, Mrabu E, Wakibia JG. 2014. Cultivation and utilisation of red seaweeds in the Western Indian Ocean (WIO) Region. J Appl Psychol 26 (2): 699-705. DOI: 10.1007/s10811-013-0086-4.
Nan C, Zhang H, Lin S, Zhao G, Liu X. 2008. Allelopathic effects of Gracilaria salicornia on selected species of harmful bloom-forming microalgae in laboratory cultures. Aquat Bot 89 (1): 9-15. DOI: 10.1016/j.aquabot.2008.01.005.
Naqvi SA, Sherazi TA, Hassan SU, Shahzad SA, Faheem Z. 2022. Anti-inflammatory, anti-infectious and anti-cancer potential of marine algae and sponge: A review. Eur J Inflamm 2022: 20. DOI: 10.1177/20587392221075514.
Nejrup LB, Staehr PA, Thomsen MS. 2013. Temperature-and light-dependent growth and metabolism of the invasive red algae Gracilaria vermiculophylla–a comparison with two native macroalgae. Eur J Phycol 48 (3): 295-308. DOI: 10.1080/09670262.2013.830778.
Phooprong S, Ogawa H, Hayashizaki K. 2007. Photosynthetic and respiratory responses of Gracilaria salicornia (C. Ag.) Dawson (Gracilaria les, Rhodophyta) from Thailand and Japan. J Appl Psychol 19 (6): 795. DOI: 10.1007/s10811-007-9194-3.
Platt T, Gallegos CL, Harrison WG. 1980. Photoinibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38: 687-701.
Pribadi TWK, Kanza AA. 2017. Tide pools diversity in Bojonglarang-Jayanti Nature Reserve, West Java, Indonesia. Ocean Life 1: 43-48. DOI: 10.13057/oceanlife/o010201.
Ramah S, Bhagooli R, Kaullysing D, Bergstad OA. 2021b. Rhodolith beds (Corallinaceae, Rhodophyta): An important marine ecosystem of the Saya de Malha and Nazareth Banks. Special Issues 2/2021 – Studies on the Mascarene Plateau. Western Indian Ocean J Mar Sci 2: 171-178. DOI: 10.4314/wiojms.si2021.2.12.
Ramah S, Etwarysing L, Auckloo N, Gopeechund A, Bhagooli R, Bahorun T. 2014. Prophylactic antioxidants and phenolics of seagrass and seaweed species: A seasonal variation study in a Southern Indian Ocean Island, Mauritius. Internet J Med Update 9 (1): 27-37.
Ramah S, Gendron G, Bhagooli R, Soondur M, Souffre A, Melanie R, Coopen P, Caussy L, Bissessur D, Bergstad OA. 2021a. Diversity and distribution of the shallow water (23-50 m) benthic habitats on the Saya de Malha Bank, Mascarene Plateau. Special Issues 2/2021 – Studies on the Mascarene Plateau. Western Indian Ocean J Mar Sci 2: 69-80. DOI: 10.4314/wiojms.si2021.2.5.
Roth MS. 2014. The engine of the reef: Photobiology of the coral–algal symbiosis. Front Microbiol 5: 422. DOI: 10.3389/fmicb.2014.00422.
Sadally SB, Taleb-Hossenkhan N, Bhagooli R. 2016. Microalgal distribution, diversity and photo-physiological performance across five tropical ecosystems around Mauritius Island. Western Indian Ocean J Mar Sci 15 (1): 49-68.
Sahidi F. 2006. Antioxidants: Extraction, identification, application and efficacy measurement. Elec J Env Agric Food Chem 7 (8): 3325-3330.
Scanlan CM, Foden J, Wells E, Best MA. 2007. The monitoring of opportunistic macroalgal blooms for the water framework directive. Mar Pollut Bull 55: 162-171. DOI: 10.1016/j.marpolbul.2006.09.017.
Schreiber U, Schliwa U, Bilger W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51-62. DOI: 10.1007/BF00024185.
Setyorini HB, Maria E, Hartoko A. 2021. Distribution pattern of macro algae at Jungwok Beach, Gunungkidul District, South Java, Indonesia. Aquac Aquar Conserv Legisl 14 (1): 441-454.
Shi X, Zou D, Hu S, Mai G, Ma Z, Li G. 2021. Photosynthetic characteristics of three cohabitated macroalgae in the Daya Bay, and their responses to temperature rises. Plants 10 (11): 2441. DOI: 10.3390/plants10112441.
Singleton VL, Rossi JA. 1965. Colorimetry of total phenolics with phosphomonybdic-phosphotungstic acid reagent. Am J Enol Vitic 16: 144-158.
Smayda TJ. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42: 1137-1153. DOI: 10.4319/lo.1997.42.5_part_2.1137.
Smolina I, Kollias S, Jueterbock A, Coyer JA, Hoarau G. 2016. Variation in thermal stress response in two populations of the brown seaweed, Fucus distichus, from the Arctic and subarctic intertidal. Royal Society Open Science 3 (1): 150429. DOI: 10.1098/rsos.150429.
Somanah MJ, Abdoulraman N, Bhagooli R, Aruoma OI, Bahorun T. 2012. Assessment of phenol content and antioxidant activities of shallow-water macroalgae from Mauritius. UnivbMauritius Res J 18A: 28-53.
Stiger V, Deslandes E, Payri CE. 2004. Phenolic contents of two brown algae, Turbinaria ornata and Sargassum mangarevense on Tahiti (French Polynesia): Interspecific, ontogenic and spatio-temporal variations. Botanica Marina 47 (5): 402-409. DOI: 10.1515/BOT.2004.058.
Szabò I, Bergantino E, Giacometti GM. 2005. Light and oxygenic photosynthesis: Energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep 6 (7): 629-663. DOI: 10.1038/sj.embor.7400460.
Tagliaferro AR, Heim KE, Bobilya DJ. 2002. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13: 572-584. DOI: 10.1016/s0955-2863(02)00208-5.
Tal O, Haim A, Harel O, Gerchman Y. 2011. Melatonin as an antioxidant and its semi-lunar rhythm in green macroalga Ulva sp. J Exp Bot 62 (6): 1903-1910. DOI: 10.1093/jxb/erq378.
Taylor R, Fletcher RL, Raven JA. 2001. Preliminary studies on the growth of selected ‘green tide’ algae in laboratory culture: Effects of irradiance, temperature, salinity and nutrients on growth rate. Botanica Marina 44: 327-336. DOI: 10.1515/BOT.2001.042.
Tziveleka LA, Tammam MA, Tzakou O, Roussis V, Ioannou E. 2021. Metabolites with antioxidant activity from marine macroalgae. Antioxidants 10 (9): 1431. DOI: 10.3390/antiox10091431.
Vergeer LHT, Aarts TL, De Groot, JD. 1995. The ‘wasting disease’ and the effect of abiotic factors (light intensity, temperature, salinity) and infection with Labyrinthula zosterae on the phenolic content of Zostera marina shoots. Aquat Bot 52 (1-2): 35-44. DOI: 10.1016/0304-3770(95)00480-N.
Voskoboinikov GM, Malavenda SV, Metelkova LO. 2021. The role of algae macrophyte in bioremediation of petroleum products of the Kola Bay of the Barents Sea. Mar Biol J 6 (3): 35-43. DOI: 10.21072/mbj.2021.06.3.04.
Xiao X, de Bettignies T, Olsen YS, Agusti S, Duarte CM, Wernberg T. 2015.Sensitivity and acclimation of three canopy-forming seaweeds to UV-B radiation and warming. PloS One 10 (12): e0143031. DOI: 10.1371/journal.pone.0143031.
Yu-Qing T, Mahmood K, Shehzadi R, Ashraf MF. 2016. Gracilaria salicornia and its polysaccharides: Food and biomedical aspects. J Biol Agric Healthcare 6 (1): 140-151.
Zhang D, Beer S, Li H, Gao K. 2020. Photosystems I and II in Gracilaria salicornia are well protected from high incident sunlight. Algal Res 52: 102094. DOI: 10.1016/j.algal.2020.102094.