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017-028 Mamboya.Indd Western IndianACCUMULATION Ocean J. Mar. OF Sci. COPPER Vol. AND6, No. ZINC 1, pp. AND 17–28, QUANTUM 2007 YIELD OF BROWN MACROALGA 17 © 2007 WIOMSA Accumulation of Copper and Zinc and their Effects on Growth and Maximum Quantum Yield of the Brown Macroalga Padina Gymnospora Florence A. Mamboyaa,b*, Harischandras B. Pratapc, Matern Mtolerad, Mats Björk a a Botany Department, Stockholm University, 106 91 Stockholm, Sweden; b Department of Botany, University of Dar es Salaam, P. O. Box 35060 Dar es Salaam, Tanzania; c Department of Zoology and Wildlife Conservation, University of Dar es Salaam, P.O. Box 35064, Dar es Salaam, Tanzania; d Institute of Marine Sciences, University of Dar es Salaam, P.O. Box 668, Zanzibar, Tanzania Key words: Copper, zinc, accumulation, growth, maximum quantum yield, Padina gymnospora Abstract—Accumulation and the effects of copper and zinc on the macroalga Padina gymnospora were assessed in the laboratory after artificial exposure to copper and zinc (separately or in combination). Exposure concentrations of copper used were 0, 25, 50, 100, 500 and 1,000 µg l-1. Concentrations of zinc exposure were 0, 50, 100, 250, 1,000 and 5,000 µg l-1. The simultaneous (or combined) addition of copper and zinc (Cu+Zn) involved 25+50, 50+100, 100+250, and 500+1,000 µg l-1. Accumulation patterns were determined by measuring tissue contents of copper and zinc, while the tolerance was assessed by measuring growth rate and photosynthetic performance, as maximum quantum yield (Fv/Fm). Furthermore, the influence of major nutrients (phosphates and nitrates) on algal-metal-accumulation was estimated after additions of nitrate (1, 10 and 20 mg l-1) and phosphate (0.1, 1 and 2 mg l-1). The data obtained showed that the accumulation increased linearly with the increase in metal concentration in the growth media. However, the presence of additional nitrate and phosphate reduced both the metal accumulation and their toxic effects. Both algal growth rate and maximum quantum yields were negatively affected in proportion to the increase in metal concentrations and exposure time. At exposures to 50, 100 and 500 µg l-1 copper, inhibition in growth was greater than 50%, while an exposure to 1,000 µg l-1of zinc was needed to cause the same effect on growth and Fv/Fm. Growth rate was a more sensitive indicator of stress than maximum quantum yield in response to exposure to copper and zinc. INTRODUCTION This is possibly a result of the increased discharge of untreated industrial wastewaters and solid wastes into Heavy metals are toxic to both plants and animals the marine environment in urban areas (Daffa, 1996; and since they are not biodegradable they can Kangwe, 1999; Engdahl et al., 1998). Consequently, accumulate through the food chain eventually monitoring of these metals is of great importance, posing a serious health risk to humans and other top and there is a need to find good bio-indicators. predators (Dallinger and Kautsky, 1985; Forstner, Some marine macroalgae are reported to tolerate 1990; Kaewsarn and Yu, 2001). On the Tanzanian and to accumulate high levels of heavy metals from coast, the levels of many metals, especially copper the surrounding seawater (e.g. Bryan, 1983; Say et and zinc; have been locally elevated during recent al., 1990; Karez et al., 1994; Amado Filho et al., years (Ferletta et al., 1996; Engdahl et al., 1998). 1996; Ferletta et al., 1996; Engdahl et al., 1998), Corresponding Author: FAM E-mail:[email protected] 18 F.A. MAMBOYA ET. AL. and Padina gymnospora has a high capability of The experimental flasks were subjected to 12 hrs retaining heavy metals in cell walls (Salgado et light and 12 hrs dark cycles with fluorescent tubes al., 2005). P. gymnospora is a brown macroalga providing a photosynthetic photon flux density of widely distributed in the Zanzibar Channel and it about 120 µmol photons m-2s-1. has been used as a bio-indicator of heavy metal pollution (Ferletta et al., 1996; Engdahl et al., Experimental design for heavy metal 1998). However, to our knowledge, no laboratory exposure studies have previously investigated the metal accumulation pattern by P. gymnospora collected The macroalgae were exposed to copper in the form -1 from the Western Indian Ocean, and neither has of CuCl2 (Merck). Concentrations used in µg Cu l -1 the influence of nutrients on its metal uptake, or were 0, 25, 50, 100, 500 and 1,000 µg l . Similarly, growth and photosynthetic responses to heavy zinc was added in the form of ZnCl2 (Merck) and metal exposure, been studied. The few laboratory zinc concentrations used were 0, 50, 100, 250, -1 studies of toxicity of heavy metals to macroalgae 1000 and 5000 µg l . Exposure to a simultaneous are from temperate regions and limited information addition of copper and zinc in the growth media is available from the tropical environment. involved 25+50, 50+100, 100+250, and 500+1,000 -1 In this study, the aim was to investigate the µg (Cu+Zn) l , respectively. Six replicate flasks response of the tropical P. gymnospora exposed were run for each treatment. The seawater was to different levels of individual and combination changed twice a week with the metal concentration of copper and zinc, using experimental metal as previously added. concentrations comparable to those found naturally The exposure experiments lasted 21 days, after in the field including more extreme concentrations which samples were collected from each flask and representative of polluted areas. As the presence washed with de-ionised water to remove salts. of major nutrients in the seawater could reduce Newly developed, young algal thalli tips (~2 cm metal accumulation and its impact on macroalgae from the growing ends of the blades) were separated (Haglund et al., 1996), the influence of nitrates and from the old parts and oven dried at 60°C until phosphates on metal accumulation and toxicity were attaining a constant weight. Such prepared samples also investigated. were analysed for copper and zinc as reported in Engdahl et al., (1998) using Inductively Coupled MATERIALS AND METHODS Plasma Optical Emission Spectrometer (ICP-OES, Spectro, Marlborough, MA, USA). The analytical quality assurance was evaluated using the Certified Culture conditions Standard Reference Material (Ulva lactuca, BCR 276), Community Bureau of Reference. Healthy, young (~5 cm long and 3 cm wide) thalli of Padina gymnospora were collected near Bawe Effect of nitrate and phosphate on Island, Zanzibar, a location relatively free from accumulation of copper and zinc land based pollution (Kangwe, 1999). They were then kept in temperature-controlled laboratory Macroalgae growing in a media containing either -1 -1 facilities of the Institute of Marine Sciences (IMS), 500 µg Cu l or 1000 µg Zn l were exposed to three Zanzibar and cultivated in 4 litre glass flasks different concentrations of nitrate and phosphate. containing 0.2 µm filtered natural seawater with Sodium nitrate (NaNO3, Merck, Darmstadt, F.R. pH 8.0, temperature 26 ºC, salinity 36 psu, nitrate Germany) and hydrous sodium hydrogen phosphate -1 -3 (NaHPO .12H O, Merck, Darmstadt, F.R. Germany) 4.7 μg-at, NO3-N l , phosphate 0.26 μg-at PO4 -P 4 2 l-1, zinc 2.9 μg.l-1 and copper 1.1 μg.l-1. The algal were used as sources of N and P, respectively. Three stocking density was about 4±0.5 g.l-1. The selected different nitrate and phosphate concentrations algae were acclimated to culture conditions for were tested, namely high nutrient (HN), with 20 -1 -1 24 hours before being exposed to copper or zinc. mg l nitrate and 2 mg l phosphate; intermediate -1 -1 Each flask was aerated to provide water movement. nutrient (IN), with 10 mg l nitrate and 1 mg l ACCUMULATION OF COPPER AND ZINC AND QUANTUM YIELD OF BROWN MACROALGA 19 of phosphate and low nutrient (LN), with 1 mg Analyser (PEA, Hansatech Instruments Ltd, Lynn, l-1 nitrate and 0.1 mg l-1 phosphate. Six replicates Norfolk, UK). Thalli were dark-adapted for about of each treatment were used to asses the effect 15 minutes before measurements were taken and of nitrate and phosphate on metal accumulation. on completion of the measurements, Fv/Fm were Control flask C1 had no metal addition while C2 automatically calculated from the recorded Fo and had 500 µg Cu l-1 or 1,000 µg Zn l-1 but without Fm data (for details see e.g. Beer and Björk 2000; additional nitrate or phosphate. Beer et al., 2001). Growth rate (DGR) Effective concentration at 50% inhibition (EC 5 0 ) and no observable effect The daily growth rate (DGR) was estimated using concentrations (NOEC) the formula DGR%= (Wt/Wo)1/t-1) * 100, where DGR% represents daily growth rate as a percentage, The DGR and Fv/Fm values expressed as percentage Wt represents fresh weight at time t, Wo is initial of the control were plotted against the logarithm of fresh weight and t is time in days (see Haglund et the exposure concentrations A line was fitted to the al., 1996). Wt was estimated after 4, 7, 14 and 21 plotted individual values using linear regression days of exposure. Weights were measured within analysis. EC50, is the effective concentration of an ample time to avoid drying of the thalli using a the toxicant causing 50% inhibition and NOEC standard weighing balance. Before measuring the is the highest concentration of toxicant with no weight of the plant, excess water was removed by observable effect (Modified from Haglund et al., blotting off using soft tissue paper. 1996). EC50 and NOEC values were determined for 7 and 21days for copper and zinc exposure Maximum quantum yield (Fv/Fm) using the dose response diagram.
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