Removal of Cypermethrin with Seaweed Gracilaria lemaneiformis

WANG Zhaohui, and YUE Wenjie

College of Life Science and Technology, Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong

Higher Education Institutes, Jinan University, Guangzhou 510632, P. R. China

Removal of Cypermethrin with Seaweed Gracilaria lemaneiformis

WANG Zhaohui*, and YUE Wenjie

College of Life Science and Technology, Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong

Higher Education Institutes, Jinan University, Guangzhou 510632, P. R. China

© Ocean University of China, Science Press and Spring-Verlag Berlin Heidelberg 2015

The removal of cypermethrin with a red macroalga, Gracilaria lemaneiformis, was studied under laboratory conditions. Results showed that the residue contents with G. lemaneiformis were significantly lower than those corresponding groups without the algal thalli after 96 h treatment. The removal rates decreased with increasing concentrations, which were about 50% without G. lemaneiformis after 96 h exposure, and increased to 89%, 73%, and 66% in flasks with G. lemaneiformis at the concentrations of 10, 100, and 1000 μg L-1, respectively. The amount of biosorption (absorption and adsorption) by G. lemaneiformis increased with the increasing concentration and exposure time. Adsorption was the main process for the removal by G. lemaneiformis, which accounted for 75%–97% of the total biosorption. However, biosorption only contributed 0.5%–19.3% to the total losses of cypermethrin, which was more efficient under the low concentration. Natural losses contributed the largest portion of losses, which was over 65% in all treatments during the experiment. The unknown pathway of removal, which might be the bio-decomposed by microorganisms attaching the algal thalli, also contributed a lot to the total removal. The results suggested that cultivation of G. lemaneiformis could significantly remove cypermethrin, especially at low concentrations, and large-scale cultivation of G. lemaneiformis has considerable potential of biorestoration of eutrophic and cypermethrin-polluted coastal sea areas.

cypermethrin; Gracilaria lemaneiformis; removal; biosorption; marine environment

1 Introduction

Cypermethrin, α-cyano-3-phenoxybenzyl-3,2,(2-dimethyl 2-2-dichlorovinyl)-2,2-cyclopropane carboxylate, is one of the important pyrethroid insecticides deemed effective for insect control both in agriculture and in homes. The use of cypermethrin has increased sharply in recent years because of the restrictions of the highly toxic organophosphate pesticides. It has, therefore, become one of the dominant insecticides in retail sales (Weston et al., 2009). However, pyrethroids including cypermethrin are highly toxic to fish and aquatic invertebrates (Clark et al., 1989). In fish culture cypermethrin is used against lice infestation (Hart et al., 1997) and its wide use has led to an increased contamination in aquatic systems.

Cypermethrin, which is regarded as a potential human carcinogen by the Environmental Protection Agency (EPA) of USA (Zhang et al., 2010), is neuro- (Wolansky and Harrill, 2008), immuno- (Jin et al., 2011), geno-(Ansari et al., 2011), and reproduction-toxic (Wang et al., 2011), and affects the endocrine system (McKinlay et al., 2008). These concerns about aquatic ecosystems and human health make it important to pave an effective and safe way of removing cypermethrin from aquatic envi-ronments.

Gracilaria lemaneiformis (Bory) Dawson, Acleto et Foldvik is a red macroalga cultivated on a large scale along the northern and southern coasts of China. It is a source of a valuable polysaccharide, agar. It is highly adaptable to temperatures, has a rapid growth rate, and grows easily by vegetative reproduction. These advantages make it a favorable candidate for mariculture (Fei, 2004). G. lemaneiformis has high nutrient bioremediation efficiency (Yang et al., 2006), and can significantly inhibit the growth of harmful algal bloom (HAB) species such as Heterosigma akashiwo (Wang et al., 2009), Scripssiella trochoidea and Chaetoceros curvisetus (Liu et al., 2006). It has, therefore, been suggested as a potential candidate for bioremediation in marine environments (Zhou et al., 2006).

In a previous study, we found that G. lemaneiformis is much less sensitive to cypermethrin than fish, aquatic invertebrates and microalgae (Wang et al., 2010b). Thus, it seems feasible that it could remove or reduce cypermethrin contamination. The purpose of this study was to evaluate the potential of G. lemaneiformis cultivation in pesticide bioremediation.

2 Materials and Methods

2.1 Collection and Cultivation of G. lemaneiformis

G. lemaneiformis was collected in April 2007 from itsfarming place at Nanao Island (116.6˚E, 23.3˚N), Shantou, China. Healthy thalli were selected, and transported to laboratory within 6 h in an insulated cooler (6–10℃). The macroalgal culture were maintained in a controlled environment chamber for one week in glass aquaria containing autoclaved (121℃, 20 min), filtered natural seawater (salinity about 32), enriched with f/2 medium (Guillard, 1973) at (20 ± 1)℃, under 100 μmol photon m-2s-1of cool-white fluorescent illumination with a dark: light cycle of 12 h:12 h. The seawater was vigorously aerated with ambient air and half of the amount was changed daily.

2.2 Chemicals

A commercial form of cypermethrin was obtained from Liwei Chemical Plant, China (EC, cypermethrin 10%, 8% agricultural emulsifier No. 2201 and 82% dimethylbenzene). The actual amount of cypermethrin in the emulsion was 91.1 g L-1determined by GC/MS analysis. Cypermethrin was preserved at 4℃. Stock solutions were prepared by diluting cypermethrin in acetone to give the nominal concentrations of 10, 100, and 1000 mg L-1according to the measured actual concentration. The analytical standard of cypermethrin for GC/MS was purchased from Sigma-Aldrich Company, USA (≥98%, for HPLC). Other chemicals were at analysis or chromatography analysis grade.

2.3 Experimental Design

Three concentrations of 10, 100, and 1000 μg L-1were set based on our previous study, which included the concentrations stimulating and inhibiting the growth of G. lemaneiformis (Wang et al., 2010b). The experiment was conducted in 3000 mL Erlenmeyer flasks containing 2000 mL f/2 medium. The initial actual concentrations of cypermethrin were determined in each concentration group before the experiment.

In the pre-experiments, we found that low or high densities of algal thalli did not benefit the growth of G. lemaneiformis. The best density for growth was 2–3 g L-1. Therefore, 2.5 g fresh weigh per liter was used in this study. In each flask, 5 g fresh weight (FW) of algal thalli was added as the treatment, while the flasks without macroalga were used as controls. Each treatment was tested in nine flasks. The flasks were incubated under the same conditions as algal cultures (See section 2.1) and agitated by hand three times daily. Dissolved oxygen (DO), pH and conductivity were measured twice a day during light and dark period each.

A 500 mL medium and 0.5 g FW of algal thalli were taken from each flask after 24, 72, and 96 h of addition of the chemical. The algal thalli were washed with large amount of distilled water (about 1 L), and the washing water and the washed algal thalli were used for the determination of cypermethrin separately. The contents of cypermethrin in the washing water and the algal thalli were defined as the adsorption and absorption amount by G. lemaneiformis, respectively.

2.4 Determination of Cypermethrin Concentrations in Medium and Algal Thalli

Cypermethrin in the medium and washing water was extracted using the solid-phase extraction (SPE) procedure described by Chen et al. (2005). A C18 SPE cartridge (Waters, USA) was conditioned with 10 mL of ethyl acetate-petroleum ether (5:95) solution, 10 mL methanol, and 10 mL distilled water, successively, with a flow rate of 2–3 mL min-1. The water sample was introduced into the cartridge at the same flow rate, and then the cartridge was vacuum-dried for 30 min to remove water. The beaker that contained the original sample was rinsed twice with a 10 mL solution of ethyl acetate-pe- troleum ether (5:95), and the solvent pumped through the cartridge. The solvent elution (20 mL) was collected and concentrated to 0.5 mL in acetone under a gentle stream of nitrogen prior to GC/MS analysis. Excess water was removed by adding baked anhydrous Na2SO4.

The algal thalli were ground on an ice bath, and the homogenates were put into a 100 mL flask. Fifty milliliter of ethyl acetate-acetone (1:1) solution was added, and let it stand on the bench for 30 min. Then the extract solution was filtered through GF/F filter. The residue was re-extracted under the same condition. The filtrates were combined, and treated as the culture samples described above.

2.5 GC/MS Analysis

For cypermethrin determination, three replicates of 1.0 μL each sample were injected splitlessly into a gas chromatography-mass spectrometry (GC/MS) column (Restek, 30 m×0.25 mm) i.d.×0.25 μm. GC/MS analysis was performed on a Shimadzu GCMS-QP2010 Plus (Shimadzu Corporation, Japan). The oven temperature was set at 80℃ for 1 min, increased at 30℃ min-1to 150℃ and then at 10℃ min-1to 280℃ and hold for 7 min. The injection port temperature was 250℃. Helium was used as the carrier gas.

A series of cypermethrin standard solutions were prepared through dilution of a stock solution of standard cypermethrin in acetone to concentrations of 10, 20, 50, 100, and 1000 μg L-1in triplicate. A close linear relationship (y =7.049×107x-2.017×106, r =0.97) was obtained between the concentration (y) and peak areas (x). Recoveries of cypermethrin from water samples were determined from standard solutions of known concentration, which were extracted and eluted at the same time as test solutions. The mean recovery ±SD of cypermethrin from water samples was 73.42% ± 14.58% (n = 6).

2.6 Data Calculation and Analysis

The percentage of removed cypermethrin (R) in solution was calculated using the equation:

where C0and Ctare the cypermethrin concentrations (μgL-1) in medium initially and at a given time t, respectively.

The cypermethrin absorbed and/or adsorbed by each gram of biomass (q) was calculated using the equation:

where C (μg mL-1) is the concentration of cypermethrin in concentrated extracts of washing water (quantity of adsorption) and/or algal thalli (quantity of absorption), V1(mL) is the volume of the extract in acetone for GC/MC analysis (0.5 mL in this study), and m1(g) is the fresh weight of the algal thalli for analysis (0.5 g in this study).

Efficiency of biosorption (E) was calculated using the following equation:

where q (μg g-1) is the amount of absorbed and adsorbed by each gram of thalli, m the fresh weight of algal thalli in each flask (5 g in this study), and V (L) the volume of reaction system (1.5 L in this study).

Mean and standard deviation (SD) were calculated for each treatment from three independent replicates. The means and standard deviations of all data were determined and graphed. Analysis of variance (ANOVA) and student’s t-test were performed to test the significance of difference among treatments using SPSS for Windows version 19.0 and the significance level was set at 0.05.

3 Results

The pH values did not change significantly during the experiment (P ＞ 0.05), which varied between 7.67 and 8.01 in flasks without G. lemaneiformis, and between 7.82 and 8.12 in flasks with G. lemaneiformis. DO values were significantly higher in flasks with G. lemaneiformis during the light period with an average of 6.61 mg L-1compared to 4.29 mg L-1in flasks without G. lemaneiformis (P＜ 0.05), while no significant difference was observed among all flasks during dark period (P ＞ 0.05). Conductivity was slightly higher in flasks without G. lemaneiformis than that with G. lemaneiformis (P ＞ 0.05).

Cypermethrin concentration reduced rapidly after the application in both flasks with and without G. lemaneiformis (Fig.1). The concentration dropped to less than one half of the initial within 96 h, after which the residue concentration was 3.79, 41.6, and 501 μg L-1in treatments without G. lemaneiformis from the initial concentrations of 10, 100, and 1000 μg L-1, respectively. The residue contents in flasks treated with G. lemaneiformis were significantly lower than those corresponding groups without the algae (P ＜ 0.05), and were 1.05, 27.3, and 343 μg L-1after 96 h treatment in the three concentrations, respectively.

Fig.1 The concentration of cypermethrin in flasks with (·) and without (○) Gracilaria lemaneiformis at initial concentrations of 10 μg L-1(a), 100 μg L-1(b), and 1000 μg L-1(c).

The removal rates (R) and efficiencies (E) of cypermethrin in flasks with and without G. lemaneiformis decreased with increasing concentration of cypermethrin (Fig.2). Furthermore, the differences in removal rate between treatments with G. lemaneiformis and without G. lemaneiformis decreased with increasing concentration. However, the final removal rates were more than 50% in all experiment groups. The removal efficiencies were 14%–28% higher in flasks with G. lemaneiformis than those without G. lemaneiformis after 96 h treatment.

Fig.2 The removal rate (R) of cypermethrin in flasks with (·) and without (○) Gracilaria lemaneiformis at initial concentrations of 10 μg L-1(a), 100 μg L-1(b), and 1000 μg L-1(c).

The amount of biosorption (absorption and adsorption) of cypermethrin by G. lemaneiformis (q) increased with the increased concentration of cypermethrin and the extension of exposure time (Fig.3). It was significantly lower at 10 μg L-1than those at 100 and 1000 μg L-1(P＜0.05). However, it was comparable at the concentrations of 100 and 1000 μg L-1. Absorption was very low at the beginning of exposure at all concentrations (0.01–0.04 μg g-1), and increased after 48 h exposure. The final absorption amounts were 0.08, 0.24 and 0.30 μg g-1in three concentrations, respectively. The amount of adsorption increased rapidly after 24 h exposure, and became stable between 48 h and 96 h exposure at concentrations of 100 and 1000 μg L-1, however increased constantly after 48 h exposure at 10 μg L-1. The final adsorption amounts were 0.27, 0.91 and 0.90 μg g-1in the three concentrations, respectively. Adsorption was the main process for biosorption, and accounted for 75%–97% of the total biosorption.

Fig.3 The amount of biosorption of cypermethrin (q) by Gracilaria lemaneiformis at initial concentrations of 10 μg L-1(a), 100 μg L-1(b), and 1000 μg L-1(c). ○ Adsorption+absorption; · Adsorption; ▲ Absorption.

Fig.4 The efficiency of biosorption (E) of cypermethrin by Gracilaria lemaneiformis.

With the increase in concentration, the efficiency of biosorption (E) of cypermethrin decreased (Fig.4), though the amount of biosorption (q) increased (Fig.3). The biosorption efficiency increased with the extension of exposure time at the concentration of 10 μg L-1, with the final efficiency of 19.3% obtained at 96 h of exposure. In the case of 100 μg L-1, the biosorption efficiencies ranged between 4.7% and 7.9% at 24–96 h exposure. While biosorption efficiencies were less than 1% throughout the experiment at 1000 μg L-1, obviously indicating that 1000 μg L-1exceeded the saturation limit of biosorption of G. lemaneiformis.

Fig.5 illustrates the profiles of cypermethrin removal in flasks with G. lemaneiformis at the three concentrations. The natural losses, which are the losses in flasks without G. lemaneiformis, contributed the largest amount of removal, which was over 65% in all treatments during the experiment with the highest proportion of 94.2% in the concentration of 100 μg L-1after 24 h exposure. The unknown pathway of removal (unknown disappearance) was especially high at high concentrations, which accounted for 11.3%–25.9%, 1.1%–18.5%, and 22.4%–27.5% of the total removal at the concentrations of 10, 100, and 1000 μg L-1, respectively. Biosorption (absorption and adsorption) by G. lemaneiformis contributed the least to,the total removal with 7.3%–19.3%, 4.7%–7.9%, and 0.5%–0.9% in the three exposure concentrations, respectively.

Fig.5 Profiles of cypermethrin removal in flasks with Gracilaria lemaneiformis at initial concentrations of 10 μg L-1(a), 100 μg L-1(b), and 1000 μg L-1(c). GL: Gracilaria lemaneiformis.

4 Discussion

Though synthetic pyrethroid pesticides have low toxicity to mammals, they are highly toxic to aquatic organisms, e.g. the half lethal concentrations (LC50) of cypermethrin to fish are 1–10 μg L-1, and less than 0.1 μg L-1to aquatic crustaceans (Clark et al., 1989). In mariculture, cypermethrin is used against sea lice infestation (Hart et al., 1997), and the recommended treatment regimen is 5 μg L-1(Medina et al., 2004). Predicted environmental concentrations of cypermethrin in sea water were estimated to be 0.02–3 μg L-1following a single application (Friberg-Jensen et al., 2003). Trace quantity of cypermethrin (0.11–1.30 μg L-1) was detected in natural sea waters of fish culturing area as well (Wang et al., 2010a). Cypermethrin levels in natural sea waters produce potential negative effects on the aquatic ecosystems, particularly for aquatic invertebrates (Medina et al., 2004), and would result in changes in plankton community structure as well (Wang et al., 2012).

Previous experiments with pyrethroids have reported that a large proportion (＞60%) of these insecticides may remain absorbed onto the glassware walls of the tubes (Ali and Baugh, 2003; Rodríguez-Liébana et al., 2011). Cypermethrin is stable under acidic or neutral conditions (pH 3–7) but hydrolyses in strongly alkaline media (pH 12–13), and it decomposes above 220℃ (WHO, 1992). Furthermore, cypermethrin has low volatility, and is stable in air and light (WHO, 1992). The environmental parameters in our experiment such as temperature (20℃), pH (7.67–8.12), and light intensity (100 μmol photon m-2s-1) were within the ranges for keeping its stability. Therefore, the contributions of natural degradation and evaporation to its losses are very low. The natural losses (＞ 50%) in flasks without G. lemaneiformis in this study might be mostly due to sorption process. Medina et al. (2002) reported that concentrations of cypermethrin in water samples decreased significantly from 3.14 μg L-1to 2.04 μg L-1after 4 days experiment. The rapid decrease of cypermethrin was observed in our previous study (Wang et al., 2010b), in which about 20% of cypermethrin was lost in 24 h and over 50% in 96 h. The pH and conductivity values changed less in flasks with and without G. lemaneiformis during the experiment. Further it is reported that the extent of absorbed pyrethoid on the laboratory glassware was independent of pH and ionic strength (Ali and Baugh, 2003). Therefore, the natural losses of cypermethrin should not show significant variations in flasks with and without G. lemaneiformis.

Marine macroalgae were reported to be effective biosorbers of heavy metals (El-Sikaily et al., 2007) and the phenoxyalkanoic acid herbicides (Ata et al., 2012). However the macroalgae used in these studies were dried or chemically activated materials. Here, we used the fresh filaments to evaluate the efficiency of G. lemaneiformis cultivation in cypermethrin removal. Though the test concentrations in this study (10–1000 μg L-1) were much higher than the background levels in the natural sea waters (Friberg-Jensen et al., 2003; Wang et al., 2010a), the high pesticide loading provided some valuable information. Adsorption was the main process of cypermethrin removal by G. lemaneiformis (Fig.3) due to its long filaments and high surface area. The maximum biosorption amounts were comparable at concentrations of 100 and 1000 μg L-1with the maximum adsorption and absorption capacity of about 0.9 and 0.3 μg g-1(Figs.3b, 3c), respectively. The results indicated that 1.2 μg g-1might be the saturation point for cypermethrin biosorption (qmax), and 100 μg L-1was the saturation limit of biosorption of G. lemaneiformis. The capacity of biosorption is highly dependent on the available adsorption sites which are determined by the morphology and physiology of the alga. The surface area of algal filaments, the lipid content of cell membranes and the composition of cell walls (Tang et al., 1998) are all important.

As the algal thalli in this study were not sterilized, though the test vessels and medium were bacteria free, the effect of bacteria in the phycosphere coexisting with G. lemaneiformis in the culture systems need to be considered. It is reported that many bacteria have the abilities of cypermethrin degradation (Chen et al., 2012; Zhao et al., 2013). Twenty percent of cypermethrin removal was by unknown mechanisms (Fig.5). This part of removal was possibly due to the biodegradation by microorganisms attached to the algal filaments. Though the bacterial community in the phycosphere may change depending on different cultural conditions and macroalgal species, it was reported that the bacteria attached at the algal thalli showed no significant difference among macroalgal species from different culturing areas and conditions, which were dominated by Pseudoalteromonas spp. (Wu, 2012). Bacteria for cypermethrin biodegradation were mostly isolated from soils and sediments, including those in Bacillus, Streptomycete and Alphaproteobacteria (Chen et al., 2012; Zhao et al., 2013), few in Pseudoalteromonas. The degradation of cypermethrin was mostly studied in co-cultures of a single bacterial species or two or three combined species under laboratorial conditions (Chen et al., 2012; Ma et al., 2013), and the biodegradation of cypermethrin by the natural bacterial community has not been studied yet. Therefore, further studies are needed to understand the contribution of biodegradation by attached bacteria in the thalli of G. lemaneiformis.

G. lemaneiformis is one of the most attractive candidates for intensive seaweed culture in China because of its high yields of valuable products, such as agar and aquaculture fodder. The annual production of G. lemaneiformis is more than 100 hundred thousand tons (dry weight) in China in 2006 (the Yearbook of Fisheries of People’s Republic of China, 2006). As a bioremediator, G. lemaneiformis growth should not be influenced by the pollutants and no significant bioconcentration should occur. The results of our previous study showed that low concentrations of cypermethrin (＜100 μg L-1) did not in-hibit the growth of G. lemaneiformis (Wang et al., 2010b). The results obtained in this study showed that G. lemaneiformis was capable of removing cypermethrin effectively, especially at low concentrations of cypermethrin, with a biosorption efficiency of 19.3% (Fig.4). Cypermethrin is easily bio-decomposed in natural environments (Chen et al., 2012), and would not therefore have lasting effects on G. lemaneiformis. Our studies suggested that cultivation of G. lemaneiformis could significantly remove cypermethrin especially under low concentrations. Considering G. lemaneiformis also has high capacity in nutrient bioremediation (Yang et al., 2006), and could effectively inhibit the growth of HAB species (Yang et al., 2006; Wang et al., 2009), large-scale cultivation of G. lemaneiformis has considerable potential in biorestoration of eutrophic and cypermethrin-polluted coastal sea areas.

Acknowledgements

The authors gratefully acknowledge Dr. Larry B. Liddle of Long Island University, USA for reviewing the manuscript. The work was financially supported by the National Key Technology R & D Program (No. 2012BA C07B05), and by the National Natural Science Foundation of China (No. 41276154).

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(Edited by Qiu Yantao)

(Received December 24, 2013; revised January 27, 2014; accepted April 27, 2015)

J. Ocean Univ. China (Oceanic and Coastal Sea Research)

DOI 10.1007/s11802-015-2567-3

ISSN 1672-5182, 2015 14 (5): 858-864

http://www.ouc.edu.cn/xbywb/

E-mail:xbywb@ouc.edu.cn

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E-mail: twzh@jnu.edu.cn