Effects of Varying Copper Concentrations on
Photosynthesis of Gracilaria salicornia
and Padina sanctae-crusis

Jesrelljane J. Aaron* and Danila T. Dy

Marine Biology Section, University of San Carlos, Cebu City, Philippines
*Bohol Island State University, Philippines

corresponding author: This email address is being protected from spambots. You need JavaScript enabled to view it.


Two tropical macroalgae, Gracilaria salicornia and Padina sanctae-crusis, were exposed to varying concentrations of total Cu and subsequently subjected to photosynthesis-irradiance (P-I) response experiments. The study aimed to determine the effects of total Cu toxicity on the P-I model parameters and growth rate of the macroalgae. The photosynthetic efficiency (α) showed a decreasing pattern with increasing total Cu concentration. Light saturation (Ik) for both algae increased at lower concentration and showed transient shift at 12.5 µg total Cu L-1. The maximum photosynthesis (Pmax) of P. sanctae-crusis was higher in specimens exposed to 12.5-25 µg total Cu L-1 compared to the controls. Unlike P. sanctae-crusis, G. salicornia exposed total Cu-free medium as well as those at 12.5-25 µg total Cu L-1 were comparable. But, both algae showed decreasing Pmax values from 50-500 µg total Cu L-1. Respiration (R) showed non-linear pattern due to some delay of the effect of copper on the respiratory system. Growth data proved to be more sensitive to total Cu with the reductions of mean daily growth rate starting at 12.5 µg total Cu L-1 for G. salicornia and negative growth rate at 500 µg total Cu L-1 for P. sanctae-crusis. After 7 days of exposure the EC20 for G. salicornia and P. sanctae-crusis were 100 and 50 µg total Cu L-1, respectively. The results suggested severe impact of total Cu+ at high concentrations on P-I parameters and growth rate of G. salicornia and P. sanctae-crusis.


Copper (Cu) is an essential micronutrient for all photosynthetic organisms (i.e. cyanobacteria, algae, and plants) and plays an important role in numerous metabolic and physiological processes (Bernal et al., 2006). However, at elevated concentrations, Cu can inhibit a large number of enzymes and interferes with several aspects of plant biochemistry, including photosynthesis, pigment synthesis, and membrane integrity (Fernandes and Henriques, 1991). . . . . read more


AALDERLINK RH, JOVIN R. 1997. Estimation of the photosynthesis/irradiance curve parameters from light and dark bottle experiments. J Plankton Res 19(11): 713-1742.
AKAIKE H. 1981. Likelihood of a model and information criteria. J Econometrics 16(1):3-14.
BERNAL M, RAMIRO MV, CASES R, PICOREL R, YRUELA I. 2006. Excess copper effect on growth, chloroplast ultrastructure, oxygen evolution activity and chlorophyll fluorescence in Glycine max cell suspensions. Physiologia Plantarum 127 (2):312-325.
BINZER T, SAND-JENSEN K. 2002. Importance of structure and density of macroalgae communities (Fucus serratus) for photosynthetic production and light utilisation. Mar Ecol Prog Ser 235:53-62.
BROWN MT, NEWMAN JE. 2003. Physiological responses of Gracilariopsis longissima (S. G. Gmelin) Steentoft, L. M. Irvine and Farnham (Rhodophyceae) to sub-lethal copper concentrations. Aquat Toxicol 64: 201-213.
CARMEN B, PÉREZ-LLORÉNS JL, VERGARA JJ. 2009. Photosynthesis and growth in macroalgae: linking functional-form and power scaling approaches. Mar Ecol Prog Ser 377:113-122.
CID, A., C. HERRERO, E. TORRES, AND J. ABALDE. 1995. Copper toxicity on the marine microalga Phaeodactylum tricornutum: effects on photosynthesis and related parameters. Aquat Toxicol 31:165-174.
CONNAN, S., AND STENGEL, D. B. 2011. Impacts of ambient salinity and copper on brown algae: 1. Interactive effects on photosynthesis, growth, and copper copper accumulation. Aquat Toxicol 104: 4-107.
COSBY BJ, HORNBERGER GM, KELLY MG. 1984. Identification of photosynthesis-light models for aquatic systems. II. Application to a macrophyte dominated stream. Ecol Modelling 23:25-51.
COX TE, SMITH CM. 2015. Photosynthetic rapid light curves for Padina sanctae-crucis vary with irradiance, aerial exposure, and tides in Hawaii’s micro-intertidal zones. Mar Biol 162(5):1061-1076.
DHARGALKAR VK, PEREIRA N. 2005. Seaweed: promising plant of the millennium. Sci and Cult 71 (3-4):60-66.
FERNANDES JC, HENRIQUES FS. 1991. Biochemical, physiological, and structural effects of excess copper in plants. Bot Rev 57(3):246-273.
GANZON-FORTES ET, AZANZA-CORALES R, ALIAZA T. 2009. Comparison of photosynthe-tic responses of healthy and ‘diseased’ Kappaphycus alvarezii (Doty) Doty using P vs I curve. Bot Mar 36 (6):503-506.
GERALDINO PJL, LIAO LM, BOO SM. 2005. Morphological Study of the marine algal genus Padina (Dictyotales, Phaeophyceae) from Southern Philippines: 3 Species New to Philippines. Algae 20 (2):99-112.
HELDT HW. 2002. Three decades in transport business: studies of metabolic transport in chloroplast-a personal perspective. Photosynth Res 73:265-272.
HENLEY WJ. 1993. Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729-739.
HILL S. 1999. Total dissolved copper and mercury concentrations in innershelf waters, off Kalpakkam, Bay of Bengal. Current Science 77(4):494-497.
HOLDEN WN. (2015). Mining amid typhoons: Large-scale mining and typhoon vulnerability in the Philippines. The Extractive Industries and Society 2(3):445-461.
HUNDING C, LANGE R. 1978. Principles of ecotoxicology. In: Ecotoxicology of Aquatic Plant Communities. Butler GC. (Ed.).  Toronto, Canada: John & Wiley p239-253.
IYER R, DE CLERCK O, COYNE VE. 2004. Morphological and taxonomic  studies of Gracilaria and Gracilariopsis species (Gracilariales, Rhodophyta) from South Africa. S. Afr. J. Bot. 70(4):521-539.
JASSBY AD, PLATT T. 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21 (4): 540-547.
JOHNSON JB, OMLAND KS. 2004. Model selection in ecology and evolution. Trends in Ecol Evol 19(2): 02-107.
JUNEAU P, DEWEZ D, MATSUI S, KIM S, POPOVIC R. 2001. Evaluation of different algal species sensitivity to mercury and metolachlor by PAM-fluorometry. Chemosphere 45(4-5):589-598.    
KUMAR KS, GANESAN K, RAO PVS. 2008.  Antioxidant potential of solvent extracts of Kappaphycus alvarezii (Doty) and edible seaweed. Food Chem 107:289-295.
KÜPPER H, GOTZ B, MIJOVILOVICH A, KÜPPER FC, MEYER-KLAUCKE W. 2009. Complexation and toxicity of copper in higher plants. I. Characterization of copper accumulation, speciation, and toxicity in Crassula helmsii as a new copper accumulator. Plant Physiol 151(2):702-714.
KÜPPER H, KÜPPER F SPILLER M. 1998. In situ detection of heavy metal substituted chlorophylls in water plants. J Exp Bot Photosynth Res 58:125-133.
KÜPPER H, ŠETLÍK I, SETLIKOVA E, FERIMAZOVA N, SPILLER M, KÜPPER FC. 2003. Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda. Funct Plant Biol 30:1187-1196.
KÜPPER H, ŠETLÍK I, SPILLER M, KÜPPER FC, PRÁŠIL O. 2002. Heavy metal-induced inhibition of photosynthesis: target of in vivo heavy metal chlorophyll formation. J  Phycol 38: 429-441.
LANARAS T, MOUSTAKOS M, SYMEONIDIS L, DIAMANTOGLOU S, KARATAGLIS S. 1993. Plant metal content, growth responses and some photosynthetic measurements on field cultivated wheat growing on ore bodies enriched in Cu. Physiol Plant 88:307-314.
LEHOTAI N, PETO A, WEISZ M, ERDEI L, KOLBERT Z. 2011. Generation of reactive oxygen and nitrogen species in pea cultivars under copper exposure. Acta Biol 55(2):273-278.
LEVY JL, ANGEL BM, STAUBER JL, POON WL, SIMPSON SL, CHENG SH, JOLLEY DF. 2008. Uptake and intenalisation of copper by three marine microalgae: comparison of copper sensitive and copper tolerant species. Aquat Toxicol 89:82-93.
LEVY JL, STAUBER JL, JOLLEY DF. 2007. Sensitivity of microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Sci Total Environ 387:141-154.
LI X, WAI OW, LI YS, COLES BJ, RAMSEY MH, THORNTON I. 2000. Heavy metal distribution in sediment profiles of the Pearl River estuary, South China Appl Geochem 15(5):567-581.
LICHTENTHALER HK. 2007. Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res 92(2):163-179.
LIDON FC, RAMALHO JC, HENRIQUEZ FS. 1993. Copper inhibition of rice photosynthesis. J Plant Physiol 142(1):12-17.
MAMBOYA F, LYIMO TJ, LANBERG T, BJORK M. 2009.  Influence of combined changes in salinity and copper modulation on growth and copper uptake in the tropical green macroalga Ulva reticulate. Estuar. Coast. Shelf Sci 84:326-330.
MARSAC NT. 2003. Phycobiliproteins and phycobilisomes: the early observations. Photosynth Res 76: 197-205.
MIJOVILOVICH A, LEITENMAIER B, MEYER-KLAUCKE PM, KRONECK PMH, GOTZ B, KÜPPER H. 2009. Complexation and toxicity of copper in higher plants II: different mechanisms for copper versus cadmium detoxification in the copper–sensitive cadmium/ zinc hyperaccumulator Thlaspi caerulescens (Ganges Ecotype). Plant Physiol 151: 15-731.
MISHRA SR. 2004. Photosynthesis in plants. Discovery Publishing House, New Delhi, India:  p.296
MORGAN-KISS RM, PRISCU JC, POCOCK T, GUDYNAITE-SAVITCH L, HUNER NPA. 2006. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environment. Microbiol Mol Biol Rev 70(1):222-252.
MULLER P, XIAO-PING L, NIYOGI KK. 2001. Non-photochemical quenching: a response to excess light energy. Plant Physiol 125: 1558-1566.
NIELSEN HD, NIELSEN SL. 2010. Adaptation to high light irradiances enhances the photosynthetic Cu2+ resistance in Cu2+ tolerant and non-tolerant populations of the brown macroalga Fucus serratus. Mar Pollut Bull 60:710-717.
NIELSEN HD, BROWNLEE C, COELHO SM, BROWN MT. 2003. Inter-population differences in inherited copper tolerance involve photosynthetic adaptation and exclusion mechanisms in Fucus serratus. New Phytol 160:157-165.
[OECD] Organization for Economic Cooperation and Development. 2002. Proposal for Updating Guideline 201 “Freshwater Algae and Cyanobacteria, Growth inhibition test”. France: Organization for Economic Cooperation and Development pp.7-8.
OLIVIER D. 2012. Antioxidant activity of plant phenols: chemical mechanisms and biological significance. Curr Org Chem 16(6):692-714.
ORTIZ AT, TRONO GC JR. 2000. Growth and reproductive pattern of intertidal and subtidal Sargassum (Sargassaceae, Phaeophyta) populations in Bolinao, Pangasinan. Science Diliman 12(2):45-50.
OUZOUNIDOU G. 1996. The use of photoacoustic spectroscopy in assessing leaf photosynthesis under copper stress: correlation of energy storage to photosystem II fluorescence parameters and redox change of P700. Plant Sci 113:229-237.
OUZOUNIDOU G, MOUSTAKAS M, STRASSER RJ. 1997. Sites of action of copper in the photosynthetic apparatus of maize leaves: kinetic analysis of chlorophyll fluorescence, oxygen evolution, absorption changes and thermal dissipation as monitored by photoacoustic signals. Aust J Plant Physiol 24:81-90.
PASICHNAYA YA. 2002. Toxicity of copper for hydrophytes: accumulation effects on photosynthesis, respiration and pigment systems. Hydrobiol J 38:103-118.
PERALES-VELA HV, GONZALEZ-MORENO S, MONTES-HORCASITAS C, CAÑIZARES-VILLANUEVA RO. 2007. Growth, photosynthetic and respiratory response to sub-lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae). Chemosphere 67:2274-2281.
PHOOPRONG, S., OGAWA, H., AND HAYASHIZAKI, K. 2007. Photosynthetic and respiratory responses of Gracilaria salicornia (C. Ag.) Dawson (Gracilariales, Rhodophyta) from Thailand and Japan. J Applied Phycol 19(6):795-801.
PRASIL O, KOLBER Z, BERRY JA, FALLOWSKI PG. 1996.  Cyclic electron flow around photosystem II in vivo. Photosynth Res 48:395-410.
RAMUS J. 1992. Productivity of seaweeds. In: Falkowski, P. G., Woodhead, A. D. (Eds.), Primary productivity and biogeochemical cycles in the sea. New York: Plenum Press p239-255.
RAYMUNDO RB. 2014. The Philippine Mining Act of 1995: Is the law sufficient in achieving the goals of output growth, attracting foreign investment, environmental protection and preserving sovereignty?. Retrieved from pdf on 17 May 2015.
SHAFER DJ, KALDY JE, SHERMAN TD, MARKO KM. 2011. Effects of salinity on photosynthesis and respiration of the seagrass Zostera japonica: a comparison of two established populations in North America Aquat Bot 95:214-220.
TELFORD WG, MOSS MW, MORSEMAN JP, ALLNUT FCT. 2001. Cyptomonad algal phycobiliproteins as fluorochromes for extracellular and intracellular antigen detec-tion by flow cytometry. Cytometry 44: 6-23.
THOMAS MA. 2001. Brown algal polyphenols: primary metabolites with multiple transitional roles. J Phycol 37(3):6.
VIANA SM, ROCHA O. 2005. The toxicity of copper sulphate and atrazine to the diatom Aulacoseira granulate (Ehrenberg) Simmons. Acta Limnol Bras 17(3):291-300.
WEHR JD. 2002. Phylum Phaeophyta. In: Freshwater Algal Flora of the British Isles. John D, Brook AJ, & Whitton BA [Eds.]. Cambridge, United Kingdom: Cambridge Univ. Press. p278-280.
WHITE A, REISKIND JB, BOWES G. 1996. Dissolved organic carbon influences the photosynthetic responses of Hydrilla to photoinhibitory conditions. Aquat Bot 53:3-13.
WOELKERLING WMJ. 1990. Biology of the red algae. In: An Introduction. Cole KM, Sheath RG. (Eds.). New York, USA: Press Syndicate p1-6.
XU Z, WU H, ZHAN D, SUN F, SUN J, WANG G. 2014. Combined effects of light intensity and NH 4+-enrichment on growth, pigmentation, and photosynthetic performance of Ulva prolifera (Chlorophyta). Chinese J of Oceanol Limnol 32:1016-1023.
YRUELA I, ALFONSO M, DE ZARATE IO, MONTOYA G, PICOREL R. 1993. Precise location of the Cu (II)-inhibitory binding site in higher plant and bacterial photosynthetic reaction centers as probed by light-induced absorbance changes. J Biol Chem 268: 1684-1689.
YRUELA I, GATZEN G, PICOREL R, HOLZWARTH AR. 1996. Cu (II)-inhibitory effect on photosystem II from higher plants: a picosecond time resolved time resolved fluorescence study.  Biochemistry 35: 9469-9474.
ZAR JH. 2010. Biostatistical analysis. New Jersey, USA: Pearson Prentice Hall 944p.