Heavy Metal Bioaccumulation and Mobility From Rice Plants to ...

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ABSTRACT Samples of soils, rice plants, and the adult, long-winged, brown planthoppers, Nilapa- rvata lugens (StÂl) (Homoptera: Delphacidae), were collected ...

PLANTÐINSECT INTERACTIONS

Heavy Metal Bioaccumulation and Mobility From Rice Plants to Nilaparvata lugens (Homoptera: Delphacidae) in China TING-LI WAN, SHUN LIU, QI-YI TANG,1

AND

JIA-AN CHENG

State Key Laboratory of Rice Biology, Institute of Insect Sciences, Zhejiang University, Yuhangtang Road, Hangzhou, 310058, China

Environ. Entomol. 43(3): 654Ð661 (2014); DOI: http://dx.doi.org/10.1603/EN13026

ABSTRACT Samples of soils, rice plants, and the adult, long-winged, brown planthoppers, Nilaparvata lugens (Stål) (Homoptera: Delphacidae), were collected from 18 sites of 9 regions in southern China. The concentrations of seven elements (Cu, Zn, As, Mo, Ag, Cd, and Pb) were measured using inductively coupled plasma mass spectrometry. Heavy metal mobility and bioaccumulation were analyzed in the rice plantÐN. lugens system. The concentrations of Zn, As, Cd, and Pb in rice plants were positively correlated with their relevant concentrations in soil samples The bioconcentration factors of the seven elements in the rice plantÐN. lugens system showed that the order of metal accumulation was Mo⬎Zn⬎Ag⬎Cd⬎Cu⬎Pb⬎As. In particular, Mo and Zn showed signiÞcantly high accumulation in N. lugens. A cluster analysis and factor analysis showed that the bioaccumulation of these seven elements in the rice plantÐN. lugens system could be classiÞed into two groups, closely related to their molar mass. The Þrst group consisted of Þve elements with relatively light molar masses: Cu, Zn, As, Mo, and Ag. Cu and Zn, which have nearly equal molar masses, showed similar accumulation levels in N. lugens. The second group included two elements with relatively heavy molar masses: Cd and Pb. This study demonstrated that bioaccumulation of seven heavy metals was regular in the rice plantÐN. lugens system. N. lugens could be used as bioindicators of the contaminated degree for Zn in rice paddy Þelds. This information may provide a basis for future ecological research on the bioaccumulation mechanism in N. lugens. KEY WORDS heavy metal, Nilaparvata lugens (Stål), bioaccumulation, molar mass

Metal elements, components of the biosphere, are commonly found in different ecological systems. The original concentrations of metal elements in the soil are determined by the lithological characteristics of parent materials and their formation processes. In the food chain, accumulation of heavy metal elements in soils may threaten plants, plant-feeding hopping insects, predators, and human beings (Heikens et al. 2001, Prince et al. 2001, Blakbern 2003). The absorption, transfer, and conversion of heavy metal elements between organisms, for example, between plants and animals, play important roles in biogeochemistry. Consequently, it is necessary to investigate the mobility and bioaccumulation of heavy metal elements in the food chain. Animals can store metals absorbed with food in speciÞc tissues or organs(Mantovi et al. 2003), or they may excrete them through the digestive system. Insects may avoid eating food with high concentrations of heavy metals, or they may excrete heavy metals directly through feces or through larval shells, epithelial cells, pupa residues, cocoons, or the external walls of galls (Helio¨ vaara and Va¨isa¨nen 1990). After enter1

Corresponding author, e-mail: [email protected]

ing an insect body, some heavy metals can be stored in tissues and organs (e.g., the digestive tract, Malpighian tubule, fat body, and epidermis) in a stable form (Ballen-Dufrancais 2002). Research has shown that some insects can accumulate large amounts of metals, which can then also be transferred to higher order organisms through the food chain (Roberts et al. 1979, Zheng et al. 2008). To date, studies on the accumulation of heavy metals in insects from contaminated ecosystems have mainly focused on the detection of heavy metal pollution in the environment (Heliovaara and Vaisanen 1990, Nummelin et al. 2007, Sun et al. 2008) or the effects of heavy metals on insects (Sun et al. 2007).Few studies have focused on the biogeochemistry of heavy metals in a soilÐplantÐinsect system (Helio¨ vaara and Va¨isa¨nen 1990, Li et al. 2006, Ashfaq et al. 2009, Zhang et al. 2009). The types, concentrations, and polluting potential of heavy metals in their food will directly affect the accumulation of heavy metals in insects (Spacies and Hamelink 1985, RothHolzapfel and Funke 1990). For example, soil insects and aquatic insects that are directly exposed to high concentrations of heavy metals, have been widely used as bioindicators for monitoring heavy metal pol-

0046-225X/14/0654Ð0661$04.00/0 䉷 2014 Entomological Society of America

June 2014

WAN ET AL.: RICE PLANTÐN. lugens HEAVY METAL BIOACCUMULATION

lution in the environment (Nehring 1976, Hawkes 1979, Borrows and Whitton 1983, Walton 1989, Van Straalen 1997, Fountain and Hopkin 2004, Ashfaq et al. 2009). Green et al.(2003)studied the biogeochemistry of different metal elements in a soilÐplantÐaphid system. Most previous studies have focused on metal accumulation either in insects that were maintained under laboratory conditions, where they were fed speciÞc heavy metals, or in insects collected from sites known to be polluted with heavy metals. To some extent, neither of those situations reßect the practical transfer and accumulation of heavy metals in a natural Þeld condition. The brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae), is one of the most common, widespread, and monophagous rice pests in Asia (Dyck and Thomas 1979). Rice is one of main food crops in China, and southern China is the worldÕs largest rice-producing area. N. lugens has received a great deal of attention because it has caused extensive damage to rice production in China. However, the current understanding with regard to the bioaccumulation of heavy metals in N. lugens is poor. Wu et al. (2003) studied the nutrient uptake of rice roots in response to an infestation of N. lugens. Azzam et al. (2010) detected the concentrations of Cu, Fe, Mn, Zn, Ca, K, Mg, and Na in both adult female N. lugens and their excreted honeydew. In addition, they reported that the concentrations of most elements, except K and Mg, in both adult females and the excreted honeydew were signiÞcantly elevated after feeding on imidacloprid-treated plants (Azzam et al. 2010). Recent studies reported that trace element concentrations could be used to identify the geographic origin of N. lugens (Peng et al. 2012), and a relationship between the concentrations of the element Eu in rice plants and in N. lugens was reported (Yang et al. 2012). Because of different ecological physiology and food chains, the biomagniÞcation of heavy metals varies in different environmental ecological systems (Goodyear and McNeill 1999). It is of great value to study the bioaccumulation of heavy metals by N. lugens from the rice plants in southern China. The aim of this study

Table 1.

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Sampling sites in nine regions of southern China

Region Yulin, Guangxi Hengnan, Hunan Hepu, Guangxi Yongfu, Guangxi Fuqing, Fujian Wan-an, Jiangxi Yifeng, Jiangxi Yongkang, Zhejiang Changde, Hunan

Sites (village)

n

Latitude

Longitude

Lianghou Liuping Kuiyang Baishui Xiayang Gancun Shihuadong Tangbao Mianting Wugang Guangming Gangkou Hongyuancao Jiangyuan Shangyang

3 3 3 9 9 3 3 3 3 3 9 3 3 3 9

22⬚ 28⬘06⬙ N 22⬚ 29⬘41⬙ N 22⬚ 44⬘07⬙ N 24⬚ 44⬘37⬙ N 24⬚ 41⬘21⬙ N 25⬚ 58⬘42⬙ N 25⬚ 00⬘39⬙ N 25⬚ 02⬘36⬙ N 25⬚ 53⬘34⬙ N 25⬚ 39⬘32⬙ N 26⬚ 29⬘34⬙ N 28⬚ 26⬘03⬙ N 28⬚ 22⬘46⬙ N 28⬚ 24⬘02⬙ N 28⬚ 53⬘09⬙ N

110⬚ 14⬘05⬙ E 110⬚ 14⬘58⬙ E 109⬚ 49⬘58⬙ E 112⬚ 35⬘36⬙ E 109⬚ 08⬘01⬙ E 110⬚ 00⬘16⬙ E 109⬚ 59⬘45⬙ E 110⬚ 00⬘55⬙ E 119⬚ 27⬘35⬙ E 119⬚ 18⬘20⬙ E 114⬚ 46⬘09⬙ E 114⬚ 33⬘09⬙ E 114⬚ 33⬘36⬙ E 114⬚ 48⬘04⬙ E 120⬚ 08⬘06⬙ E

Duijin Fengming Hongyan

3 3 3

28⬚ 56⬘07⬙ N 29⬚ 18⬘45⬙ N 29⬚ 18⬘45⬙ N

111⬚ 29⬘18⬙ E 111⬚ 20⬘53⬙ E 111⬚ 18⬘20⬙ E

was to determine concentrations of the seven moststudied metal elements in rice plants and N. lugens individuals collected from various sites in southern China. Both correlations between the metal contents in rice plants and soils and mobility of heavy metals in the rice plantÐN. lugens system were analyzed. Materials and Methods Samples. N. lugens adult samples (n ⫽ 78), rice plant samples (n ⫽ 78), and soil samples (n ⫽ 78) were collected from June to September 2010 from 18 sites in the nine target regions. The rice plant sample was the stem with sheath from 10 to 30 cm above ground, where most of N. lugens adults occur and feed. The nine regions, located in southern China, were Hepu, Yulin, and Yongfu in Guangxi Province; Hengnan and Changde in Hunan Province; Yifeng and Wan-an in Jiangxi Province; Fuqing in Fujian Province; and Yongkang in Zhejiang Province. Table 1 and Fig. 1 shows the sampling sites in the nine regions. All collected N. lugens samples were immediately stored in

Fig. 1. Map of regions in southern China where soil, rice plants, and N. lugens were sampled.

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the freezer at ⫺20⬚C until use. All N. lugens samples were dried at 50⬚C in an oven for 24 h before analysis. All of the collected rice plant and soil samples were dried at room temperature in the laboratory, after which the rice plants were shattered with a stainless crusher and stored in sealed bags before analysis. The soil samples were passed through a 2 mm sieve and stored in sealed bags before analysis. Analytical Apparatus and Reagents. Determination of mineral elements was performed using a inductively coupled plasma-mass spectrometer (ICPÐMS; Agilent 7500A, Yokogawa Analytical Systems Inc., Tokyo, Japan), equipped with an octopole reaction system. A multielement solution with nitric acid (HNO3, 2%) was obtained by mixing 65% HNO3 and 18 M⍀ highpurity deionized water (Milli-Q system, Strasbourg, Cedex, France) for external calibration. HNO3 65% Suprapur and hydrogen peroxide (H2O2) 30% Suprapur were obtained from Merck (Darmstadt, Germany). Standard solutions were prepared by diluting 1,000 mg liter⫺1 stock solutions of Mn, Mo, Cd, Ce, V, Th, Cs, Be, Tl, Fe, Nd, Pr, Se, Tm, Lu, Eu, Ho, Br, Dy, Gd, U, Sm, and Er (Agilent, Palo Alto, CA). An internal standard stock solution (6Li, 45Sc, 72Ge, 115In, 209Bi, and HNO3 10%) was obtained from Agilent. Determination of Elemental Concentrations. The contents of seven elements (Cu, Zn, As, Mo, Ag, Cd, and Pb) in each N. lugens adult, rice plant, and soil samples were evaluated. Exactly 200 mg of each dry N. lugens sample and dry rice plant sample was weighed in polytetraßuoroethylene vessels, and subjected to sufÞcient digestion with 4 ml of HNO3 (65%) and 0.5 ml of H2O2 (30%) for 2 h. Each sample was then subjected to mineralization in a dry oven (model DGX-9143B, Fuma, Shanghai, China) as follows: 600 W for 120 min at 120⬚C and 600 W for 480 min at 160⬚C. Exactly 200 mg of each soil sample was weighed in polytetraßuoroethylene vessels and subjected to sufÞcient digestion with 6 ml of HNO3 (65%) and 2 ml of hydrogen ßuoride in microwave digestion system (model Multiwave 3000, Anton Parr, Austria) as follows: 5 min at 150⬚C and 30 min at 200⬚C. Digestion was conÞrmed to be complete when no nitrous oxide gases evolved. This step was followed immediately by ventilation at room temperature, and then the solution was transferred through a medium speed Þlter. After mineralization, the samples were diluted with deionized water and transferred to a 50-ml volumetric ßask. Blank solutions were prepared with HNO3 (65%) subjected to the same procedure. The limit of detection for each of the seven elements was estimated as three times the standard deviation (SD) of the average measurement of the blank solutions. The samples of rice plants and N. lugens were analyzed using an ICPÐMS, with the following operating conditions: Rf power, 1,250 W; plasma gas ßow rate, 15.0 liters min⫺1; carrier gas, 1.06 liters min⫺1; and sample uptake rate by peristaltic pump, 0.1 revolutions per second (r/s). Statistical Analysis. Statistical analyses were conducted with the data processing system software 13.50 for Windows (Tang and Zhang 2013). The concentration of each element in rice plants and N. lugens was

Vol. 43, no. 3

expressed as the mean ⫾ SD. One way analysis of variance (ANOVA) was used to evaluate the geographic effects of heavy metal elements among the nine regions. The correction analysis was conducted to analyze the relationship of heavy metals in soils and those in rice plants. A one-sample t-test, with the null hypothesis that the population mean was equal to 1, was used to test the difference between the bioconcentration factors (BCFs) and 1. R-type cluster analysis and factor analysis were used to analyze the mobility and bioaccumulation of heavy metals in the rice plantÐN. lugens system. Results Concentrations of Heavy Metal Elements and Geographic Differences. The samples of N. lugens and rice plants from the 18 sites were subjected to ICPÐMS quantitative analysis. The mean concentrations of the seven metal elements in soils, rice plants, and N. lugens and their ANOVA analysis were shown in Table 2, Table 3, and Table 4, respectively. The distribution of heavy metals in the rice plantÐN. lugens system indicates that the concentration of Zn was highest and the concentration of Ag was lowest. The result of one-way ANOVA showed signiÞcant differences among the different sites for all seven elements in both soil samples and rice plant samples: Cu (F ⫽ 9.6265, df ⫽ 17, P ⬍ 0.0001; F ⫽ 4.9336, df ⫽ 17, P ⬍ 0.0001); Zn (F ⫽ 33.6173, df ⫽ 17, P ⬍ 0.0001; F ⫽ 5.2004, df ⫽ 17, P ⬍ 0.0001); As (F ⫽ 18.3576, df ⫽ 17, P ⬍ 0.0001; F ⫽ 3.2931, df ⫽ 17, P ⫽ 0.0004); Mo (F ⫽ 6.1527, df ⫽ 17, P ⬍ 0.0001; F ⫽ 10.4292, df ⫽ 17, P ⬍ 0.0001); Ag (F ⫽ 2.9445, df ⫽ 17, P ⫽ 0.0011; F ⫽ 2.3894, df ⫽ 17, P ⫽ 0.0072); Cd (F ⫽ 71.0525, df ⫽ 17, P ⬍ 0.0001; F ⫽ 7.6188, df ⫽ 17, P ⬍ 0.0001); and Pb (F ⫽ 44.3859, df ⫽ 17, P ⬍ 0.0001; F ⫽ 6.6070, df ⫽ 17, P ⬍ 0.0001).There were signiÞcant differences in the N. lugens samples for six elements: Zn (F ⫽ 2.5981, df ⫽ 17, P ⫽ 0.0034); As (F ⫽ 5.7699, df ⫽ 17, P ⬍ 0.0001); Mo (F ⫽ 14.007, df ⫽ 17, P ⬍ 0.0001); Ag (F ⫽ 4.4624, df ⫽ 17, P ⬍ 0.0001); Cd (F ⫽ 30.3729, df ⫽ 17, P ⬍ 0.0001); and Pb (F ⫽ 3.9189, df ⫽ 17, P ⬍ 0.0001). However, Cu (F ⫽ 1.1108, df ⫽ 17, P ⫽ 0.3655) was not signiÞcantly different among the sites for N. lugens. Correlationship of Heavy Metals Concentrations Between Rice Plants and Soils. The correlation coefÞcients between rice plants and soil of seven elements, Pb, Cd, Zn, As, Mo, Cu, and Ag, were 0.5977 (P ⬍ 0.0001), 0.5521 (P ⬍ 0.0001), 0.4563 (P ⬍ 0.0001), 0.4493 (P ⬍ 0.0001), 0.2023 (P ⫽ 0.0757), 0.0842 (P ⫽ 0.4636), and 0.0949 (P ⫽ 0.4085), respectively. The concentrations of Pb, Cd, Zn, and As in rice plants were signiÞcantly positive correlated with the relevant elements in soils. Biconcentration Factors of Heavy Metals Among Different Sites. Chemical accumulation in N. lugens was evaluated using BCF, which is deÞned as the ratio of an elemental concentration in the body of N. lugens to its concentration in the host rice plant, as follows: BCF ⫽ M BPH/M RP

June 2014 Table 2. Sites Lianghou Liuping Kuiyang Baishui Xiayang Gancun Shihuadong Tangbao Mianting Wugang Guangming Gangkou Hongyuancao Jiangyuan Shangyang Duijin Fengming Hongyan F P

WAN ET AL.: RICE PLANTÐN. lugens HEAVY METAL BIOACCUMULATION Heavy metal concentrations in soils collected from southern China (␮g/g) Mean ⫾ SD Cu

Zn

As

Mo

Ag

Cd

Pb

19.25 ⫾ 3.60 17.63 ⫾ 3.99 22.49 ⫾ 0.91 25.88 ⫾ 2.38 19.48 ⫾ 2.55 12.04 ⫾ 0.88 13.33 ⫾ 0.24 12.19 ⫾ 0.30 13.50 ⫾ 0.88 9.04 ⫾ 0.83 17.19 ⫾ 3.37 28.51 ⫾ 0.57 17.61 ⫾ 0.83 24.49 ⫾ 1.05 13.49 ⫾ 2.96 24.13 ⫾ 11.10 16.91 ⫾ 4.15 15.64 ⫾ 0.98 9.6265 ⬍0.0001

72.25 ⫾ 20.19 63.72 ⫾ 15.69 81.47 ⫾ 4.15 88.75 ⫾ 4.76 55.65 ⫾ 1.89 28.55 ⫾ 4.94 31.06 ⫾ 4.15 30.06 ⫾ 2.98 62.00 ⫾ 0.59 55.47 ⫾ 1.71 36.97 ⫾ 7.33 82.23 ⫾ 2.39 78.39 ⫾ 4.03 87.34 ⫾ 4.31 54.24 ⫾ 9.28 55.89 ⫾ 4.94 57.20 ⫾ 2.85 61.91 ⫾ 0.98 33.6173 ⬍0.0001

9.04 ⫾ 4.07 4.88 ⫾ 4.77 9.64 ⫾ 1.14 18.78 ⫾ 3.83 11.91 ⫾ 1.91 2.27 ⫾ 0.74 2.39 ⫾ 0.48 2.48 ⫾ 1.18 3.68 ⫾ 0.47 4.03 ⫾ 0.94 7.43 ⫾ 2.23 9.12 ⫾ 1.27 8.05 ⫾ 0.47 8.47 ⫾ 1.24 5.85 ⫾ 0.84 8.58 ⫾ 1.94 8.33 ⫾ 0.82 8.99 ⫾ 3.18 18.3576 ⬍0.0001

2.57 ⫾ 1.39 1.39 ⫾ 1.69 3.37 ⫾ 0.13 1.10 ⫾ 0.12 1.66 ⫾ 1.02 0.73 ⫾ 0.24 0.87 ⫾ 0.25 0.68 ⫾ 0.04 0.68 ⫾ 0.03 1.92 ⫾ 0.12 0.72 ⫾ 0.21 0.57 ⫾ 0.28 0.40 ⫾ 0.19 0.33 ⫾ 0.07 1.04 ⫾ 0.29 0.70 ⫾ 0.22 1.11 ⫾ 0.16 0.78 ⫾ 0.30 6.1527 ⬍0.0001

0.30 ⫾ 0.03 0.32 ⫾ 0.04 0.29 ⫾ 0.02 0.41 ⫾ 0.07 0.31 ⫾ 0.02 0.25 ⫾ 0.06 0.24 ⫾ 0.06 0.27 ⫾ 0.03 0.33 ⫾ 0.03 0.29 ⫾ 0.01 0.39 ⫾ 0.06 0.38 ⫾ 0.21 0.30 ⫾ 0.06 0.29 ⫾ 0.02 0.42 ⫾ 0.10 0.32 ⫾ 0.03 0.31 ⫾ 0.08 0.34 ⫾ 0.05 2.9445 0.0011

0.37 ⫾ 0.01 0.42 ⫾ 0.03 0.38 ⫾ 0.01 0.86 ⫾ 0.08 0.33 ⫾ 0.02 0.29 ⫾ 0.04 0.33 ⫾ 0.03 0.33 ⫾ 0.01 0.17 ⫾ 0.01 0.17 ⫾ 0.02 0.29 ⫾ 0.02 0.45 ⫾ 0.11 0.32 ⫾ 0.11 0.27 ⫾ 0.03 0.39 ⫾ 0.03 0.43 ⫾ 0.05 0.45 ⫾ 0.01 0.46 ⫾ 0.11 71.0525 ⬍0.0001

55.71 ⫾ 8.67 43.41 ⫾ 27.59 57.75 ⫾ 15.96 63.76 ⫾ 11.77 60.81 ⫾ 11.82 21.26 ⫾ 2.83 25.52 ⫾ 5.50 24.32 ⫾ 1.52 46.21 ⫾ 8.99 44.93 ⫾ 8.91 31.49 ⫾ 7.61 45.81 ⫾ 15.60 39.96 ⫾ 4.70 40.74 ⫾ 3.73 43.65 ⫾ 9.20 36.99 ⫾ 9.21 39.81 ⫾ 2.36 35.52 ⫾ 6.58 44.3859 ⬍0.0001

Where MBPH is the element concentration in N. lugens samples, and MRP is the element concentration in rice plant samples. The one-sample t-test indicated the difference between BCF and one for each element (Table 4). In the rice plantÐN. lugens system, the BCFs of seven elements showed the following rank order: Mo⬎Zn⬎Ag⬎Cd⬎Cu⬎Pb⬎As. The one-sample ttest showed that the BCFs of Zn and Mo were significantly ⬎1 (t ⫽ 2.74, df ⫽ 17, P ⫽ 0.0069; and t ⫽ 3.49, df ⫽ 17, P ⫽ 0.0014, respectively), and the BCFs of As and Pb were signiÞcantly ⬍1 (t ⫽ 32.01, df ⫽ 17, P ⬍ 0.0001; and t ⫽ 8.73, df ⫽ 17, P ⬍ 0.0001, respectively). This indicated that Zn and Mo were more easily transferred from the rice plant to the N. lugens through feeding than As and Pb. Bioaccumulation Characteristics of Heavy Metals in N. lugens. R-type Cluster Analysis. The R-type cluster analysis (Fig. 2) demonstrated that the bioaccumuTable 3. Sites Lianghou Liuping Kuiyang Baishui Xiayang Gancun Shihuadong Tangbao Mianting Wugang Guangming Gangkou Hongyuancao Jiangyuan Shangyang Duijin Fengming Hongyan F P

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lation characteristics of the seven elements could be classiÞed into two groups according to their molar mass. The seven elements were ranked by molar mass, in ascending order, as follows: Cu⬎Zn⬎As⬎Mo⬎Ag⬎ Cd⬎Pb. The Þrst Þve elements of lighter molar mass (Cu, Zn, As, Mo, and Ag) comprised the Þrst group; the mechanisms of accumulating Cu and Zn were most similar in N. lugens. The second group comprised Cd and Pb, with molar masses much greater than those of the Þrst group. Factor Analysis. Factor analysis is a multivariate statistical method to simplify complex relationships among variables by creating common factors. Each factor represents a cluster of interrelated variables. Seven samples were analyzed using factor analysis with a principal component method and varimax rotation. Two common factors were retained, which explained ⬇65.5% of the variance. Factor 1 explained

Heavy metal concentrations in rice plants grown in southern China (␮g/g) Mean ⫾ SD Cu

Zn

As

Mo

Ag

Cd

Pb

24.43 ⫾ 3.19 24.02 ⫾ 0.59 15.35 ⫾ 7.16 25.33 ⫾ 8.36 20.09 ⫾ 6.05 12.76 ⫾ 6.55 22.49 ⫾ 3.85 20.16 ⫾ 1.06 19.83 ⫾ 10.03 18.08 ⫾ 8.12 25.33 ⫾ 5.31 28.51 ⫾ 0.57 45.75 ⫾ 2.55 26.96 ⫾ 5.23 31.51 ⫾ 7.79 15.55 ⫾ 6.67 24.07 ⫾ 2.08 28.79 ⫾ 1.51 4.9336 ⬍0.0001

104.22 ⫾ 25.13 105.88 ⫾ 21.57 85.72 ⫾ 26.91 197.07 ⫾ 82.94 91.68 ⫾ 28.04 143.08 ⫾ 32.73 80.22 ⫾ 24.27 61.30 ⫾ 13.57 106.97 ⫾ 33.00 201.49 ⫾ 103.97 120.38 ⫾ 51.25 249.86 ⫾ 43.13 282.89 ⫾ 83.87 201.44 ⫾ 61.36 124.48 ⫾ 43.04 86.83 ⫾ 28.02 115.95 ⫾ 36.46 199.85 ⫾ 58.43 5.2004 ⬍0.0001

1.58 ⫾ 1.47 2.36 ⫾ 2.18 7.82 ⫾ 4.47 26.89 ⫾ 18.26 11.90 ⫾ 9.29 4.65 ⫾ 4.20 2.62 ⫾ 2.36 2.30 ⫾ 2.36 3.12 ⫾ 71.99 3.22 ⫾ 2.23 5.18 ⫾ 3.75 10.07 ⫾ 5.92 3.57 ⫾ 2.25 5.05 ⫾ 3.14 8.05 ⫾ 7.53 13.45 ⫾ 8.33 8.27 ⫾ 5.22 7.24 ⫾ 4.48 3.2931 0.0004

0.66 ⫾ 0.02 0.81 ⫾ 0.05 0.57 ⫾ 0.10 0.59 ⫾ 0.22 0.54 ⫾ 0.12 1.37 ⫾ 0.18 0.77 ⫾ 0.09 0.61 ⫾ 0.03 0.91 ⫾ 0.02 0.55 ⫾ 0.08 0.54 ⫾ 0.11 0.51 ⫾ 0.15 0.36 ⫾ 0.12 0.39 ⫾ 0.13 0.51 ⫾ 0.14 0.44 ⫾ 0.16 0.70 ⫾ 0.06 0.94 ⫾ 0.12 10.4292 ⬍0.0001

0.01 ⫾ 0.01 0.01 ⫾ 0.01 0.02 ⫾ 0.02 0.03 ⫾ 0.02 0.04 ⫾ 0.02 0.02 ⫾ 0 0.02 ⫾ 0.01 0.02 ⫾ 0.01 0.02 ⫾ 0 0.03 ⫾ 0.01 0.03 ⫾ 0.01 0.03 ⫾ 0.02 0.03 ⫾ 0.01 0.03 ⫾ 0.01 0.03 ⫾ 0.01 0.003 ⫾ 0.01 0.01 ⫾ 0 0.01 ⫾ 0 2.3894 0.0072

2.72 ⫾ 0.10 1.34 ⫾ 0.08 0.03 ⫾ 0.07 3.08 ⫾ 2.33 1.18 ⫾ 0.31 0.76 ⫾ 0.04 0.97 ⫾ 0.08 0.85 ⫾ 0.08 0.27 ⫾ 0.03 0.69 ⫾ 0.24 0.95 ⫾ 0.29 0.86 ⫾ 0.06 1.16 ⫾ 0.18 2.55 ⫾ 0.35 0.17 ⫾ 0.05 0.99 ⫾ 0.13 0.77 ⫾ 0.11 5.16 ⫾ 0.83 7.6188 ⬍0.0001

7.79 ⫾ 0.29 3.81 ⫾ 0.47 2.13 ⫾ 0.71 5.03 ⫾ 0.92 3.45 ⫾ 0.83 2.29 ⫾ 0.26 2.97 ⫾ 0.10 1.62 ⫾ 0.18 1.13 ⫾ 0.68 1.62 ⫾ 0.56 1.26 ⫾ 0.30 1.98 ⫾ 0.48 2.61 ⫾ 0.23 7.88 ⫾ 1.29 1.30 ⫾ 0.34 0.85 ⫾ 0.55 1.19 ⫾ 0.35 1.23 ⫾ 0.37 6.6070 ⬍0.0001

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Table 4. Sites Lianghou Liuping Kuiyang Baishui Xiayang Gancun Shihuadong Tangbao Mianting Wugang Guangming Gangkou Hongyuancao Jiangyuan Shangyang Duijin Fengming Hongyan F P

Vol. 43, no. 3

Heavy metal concentrations in N. lugens collected from southern China (␮g/g) Mean ⫾ SD Cu

Zn

25.33 ⫾ 9.05 23.30 ⫾ 7.00 31.01 ⫾ 10.17 16.49 ⫾ 6.90 18.00 ⫾ 8.47 19.87 ⫾ 9.08 14.85 ⫾ 9.22 15.79 ⫾ 8.48 19.33 ⫾ 10.34 19.22 ⫾ 11.39 25.25 ⫾ 10.12 17.69 ⫾ 1.12 21.97 ⫾ 8.62 11.90 ⫾ 0.96 20.76 ⫾ 8.05 20.72 ⫾ 9.86 23.81 ⫾ 7.56 14.61 ⫾ 9.71 1.1108 0.3655

183.43 ⫾ 42.86 158.67 ⫾ 25.46 177.12 ⫾ 32.69 191.61 ⫾ 34.86 137.25 ⫾ 21.46 196.12 ⫾ 18.96 145.59 ⫾ 1.34 145.53 ⫾ 2.33 168.23 ⫾ 33.63 168.69 ⫾ 33.83 163.23 ⫾ 35.97 199.76 ⫾ 26.67 156.34 ⫾ 15.47 138.14 ⫾ 24.85 122.91 ⫾ 32.71 142.73 ⫾ 44.88 164.96 ⫾ 32.06 145.83 ⫾ 39.34 2.5981 0.0034

As 0.70 ⫾ 0.08 0.84 ⫾ 0.18 0.98 ⫾ 0.35 4.46 ⫾ 2.40 2.25 ⫾ 1.51 0.83 ⫾ 0.17 0.72 ⫾ 0.20 0.69 ⫾ 0.06 0.99 ⫾ 0.19 0.67 ⫾ 0.19 0.91 ⫾ 0.20 0.82 ⫾ 0.03 1.06 ⫾ 0.15 1.00 ⫾ 0.03 0.83 ⫾ 0.40 0.89 ⫾ 027 1.38 ⫾ 0.18 0.56 ⫾ 0.16 5.7699 ⬍0.0001

43.5% and factor 2 explained 22.0% of the variance (Table 5). In Table 6, elements Cu, Zn, As, Mo, and Ag showed high loadings for factor 1; thus, factor 1 was associated with the elements of smaller molar mass. Elements of greater molar mass showed high loadings in factor 2. This result was in accordance with the result of the cluster analysis. In factor 1, the load coefÞcients of Cu, Zn, As, and Ag were positive, and the load coefÞcient of Mo was negative. This phenomenon indicated that the bioaccumulation activities for Cu, Zn, As, and Ag in N. lugens were synergistic, and the bioaccumulation activity between Mo and the other four elements was probably antagonistic. In factor 2, the load coefÞcient of Pb was positive and that of Cd was negative, which indicated that the bioaccumulation processes for Pd and Cd were antagonistic in N. lugens. Discussion The mobility and bioaccumulation of seven heavy metals in the rice plantÐN.lugens system were studied

Fig. 2. R-type cluster analysis for the seven elements in the rice plantÐN.lugens system. The number in the upperright corner of each element presents its molar mass.

Mo

Ag

Cd

Pb

0.81 ⫾ 0.07 0.78 ⫾ 0.06 1.16 ⫾ 0.07 0.68 ⫾ 0.20 0.52 ⫾ 0.03 1.31 ⫾ 0.06 1.07 ⫾ 0.07 1.10 ⫾ 0.09 2.87 ⫾ 1.47 1.08 ⫾ 0.01 0.97 ⫾ 0.12 2.39 ⫾ 0.20 1.85 ⫾ 0.21 0.89 ⫾ 0.08 0.92 ⫾ 0.16 1.06 ⫾ 0.27 0.84 ⫾ 0.27 1.02 ⫾ 0.18 14.0007 ⬍0.0001

0.02 ⫾ 0.01 0.02 ⫾ 0.01 0.04 ⫾ 0.02 0.04 ⫾ 0.01 0.04 ⫾ 0.01 0.03 ⫾ 0.01 0.01 ⫾ 0.01 0.02 ⫾ 0.01 0.04 ⫾ 0.02 0.02 ⫾ 0.01 0.03 ⫾ 0.01 0.01 ⫾ 0.01 0.02 ⫾ 0 0.02 ⫾ 0.01 0.02 ⫾ 0.01 0.01 ⫾ 0.01 0.02 ⫾ 0.01 0.01 ⫾ 0 4.4624 ⬍0.0001

1.39 ⫾ 0.23 1.00 ⫾ 0.09 0.21 ⫾ 0.02 2.49 ⫾ 0.51 2.41 ⫾ 0.50 1.06 ⫾ 0.26 1.47 ⫾ 0.06 1.42 ⫾ 0.06 0.20 ⫾ 0.02 0.19 ⫾ 0.01 0.55 ⫾ 0.31 0.55 ⫾ 0.05 0.42 ⫾ 0.04 1.38 ⫾ 0.15 0.33 ⫾ 0.27 1.54 ⫾ 0.37 0.44 ⫾ 0.09 1.80 ⫾ 0.33 30.3729 ⬍0.0001

1.01 ⫾ 0.31 0.80 ⫾ 0.18 0.51 ⫾ 0.22 6.70 ⫾ 5.77 0.63 ⫾ 0.25 0.56 ⫾ 0.32 0.36 ⫾ 0.18 0.37 ⫾ 0.28 0.80 ⫾ 0.02 0.54 ⫾ 0.30 0.67 ⫾ 0.40 0.42 ⫾ 0.05 0.85 ⫾ 0.11 0.56 ⫾ 0.13 0.44 ⫾ 0.26 0.65 ⫾ 0.38 0.48 ⫾ 0.23 0.28 ⫾ 0.22 3.9189 ⬍0.0001

in 18 sites from 9 regions in China. Concentrations of heavy metals vary in different parts of rice plants, and the highest concentrations occur in the root (Mo et al. 2002). Heavy metals absorbed by rice plants are always stored in rice plants, and the concentrations of metals in plant were closely related to their availability in soil, and hence it is difÞcult to measure the concentrations of their availability. Therefore, we can use the correlations between concentrations in soil and rice plants to show the mobility of heavy metals in soil-rice plant system. However, N. lugens grows rapidly, and whenever it feeds on anything containing heavy metals, they are excreted in the honeydew. Heavy metals in BPH origin from their food. It is better to use the BCFs than correlations to indicate the accumulation of heavy metals in plantÐN. lugens system. We measured concentrations of heavy metals in the portion of rice plants 10 to 30 cm above ground, where N. lugens mainly occur and feed. The results could objectively represent the relationship of heavy metals between N. lugens and their food resource. This study demonstrated that N. lugens can accumulate several metals, particularly Mo and Zn. The bioaccumulation of seven elements could be classiÞed into two groups, the Þrst group included Cu, Zn, Mo, As, and Ag with light molar masses, and the second group included Pb and Cd with greater molar masses. The concentrations of six elements in both N. lugens and rice plants showed signiÞcant geographic differences. It is possible that the abundance of heavy metals in both N. lugens and rice plants can be closely related to the soil background. Heavy metals in the bodies of N. lugens can be used as an indicator for identifying the geographic origin of N. lugens (Peng et al. 2012). It is clear that the concentrations of some heavy metals in rice plants were positive correlated with their concentrations in soils, such as Cd, As, Pb, and Zn, thereby indicating that the element contents in rice plants

June 2014 Table 5.

WAN ET AL.: RICE PLANTÐN. lugens HEAVY METAL BIOACCUMULATION

659

BCFs of seven heavy metals in N. lugens

Sites

Cu

Zn

As

Mo

Ag

Cd

Pb

Lianghou Liuping Kuiyang Baishui Xiayang Gancun Shihuadong Tangbao Mianting Wugang Guangming Gangkou Hongyuancao Jiangyuan Shangyang Duijin Fengming Hongyan Average SD t-test P

0.96 0.97 2.02 0.65 0.90 1.56 0.66 0.78 0.97 1.06 1.00 0.62 0.48 0.44 0.66 1.33 0.99 0.51 0.92 0.40 0.80 0.2179

1.76 1.50 2.07 0.97 1.50 1.37 1.81 2.37 1.57 0.84 1.36 0.80 0.55 0.69 0.99 1.64 1.42 0.73 1.33 0.51 2.74 0.0069

0.44 0.36 0.13 0.17 0.19 0.18 0.27 0.30 0.32 0.21 0.18 0.08 0.30 0.20 0.10 0.07 0.17 0.08 0.21 0.11 32.01 ⬍0.0001

1.23 0.96 2.02 1.16 0.96 0.96 1.39 1.81 3.16 1.96 1.78 4.66 5.14 2.27 1.82 2.39 1.20 1.09 2.00 1.21 3.49 0.0014

1.50 1.75 1.71 1.14 0.89 1.50 0.57 1.40 1.83 0.75 1.04 0.40 0.60 0.63 1.11 4.00 1.67 1.00 1.31 0.81 1.60 0.0642

0.51 0.74 0.71 0.81 2.03 1.38 1.51 1.66 0.76 0.28 0.58 0.83 0.36 0.54 1.90 1.56 0.56 0.35 0.95 0.56 0.38 0.3542

0.13 0.21 0.24 1.33 0.18 0.24 0.12 0.23 0.71 0.33 0.54 0.21 0.33 0.07 0.34 0.77 0.40 0.23 0.37 0.31 8.73 ⬍0.0001

were closely related to their availability in soils (Adriano 1986). As an essential element, Zn plays an important role in the metabolism at process in both plants and animals, an excessive zinc. may be toxic for organisms. Zn has received great attention because the concentrations of Zn in rice plants was positively correlated with their concentrations in soils shown in the result of the correlation of heavy metals concentrations between rice plants and soils. BCF for Zn transferred from rice plants to N. lugens was in agreement with results reported in other insects (Merrington et al. 1997b, Lindquist et al. 1992, Winder et al. 1999, Green et al. 2003). Therefore, Zn can be a target heavy metal indicator of environmental contamination monitored using N. lugens. Another study showed that N. lugens did not accumulate As or Pb, instead it released most of these minerals by excretion (Shi et al. 2011), which is consistent with our results. Pb is an important environmental contaminant with high toxicity, which attracts the interest of many researchers. It was reported that Pb accumulation in was lower in the grasshoppers than the plants they consumed (Devkotaa and Schmidt 2000). According to the load coefÞcient of Cu and Zn, we found that Cu and Zn had similar bioaccumulation Table 6. Principal factor loadings of elements for bioaccumulation in the rice plant–N. lugens system Element

Factor 1

Factor 2

Cu Zn As Mo Ag Cd Pb Variance Total variance%

0.9367 0.9281 0.5280 ⫺0.6844 0.7274 ⫺0.0055 ⫺0.1642 3.0422 43.4604

0.1696 ⫺0.2579 0.2796 0.3650 0.3537 ⫺0.9643 0.4224 1.5400 65.4606

patterns. Clearly, the molar mass of Cu and Zn (63 and 66, respectively) are similar, and Cu is next to Zn in the periodic table of elements. This suggests that the bioaccumulation mechanisms in N. lugens may be regulated by a process related to molar mass. Thus, heavy metals of similar molar masses might show similar patterns of accumulation in N. lugens, which is in accordance with the previous report that the distribution and bioaccumulation of elements in insects was closely related to their position in the periodic table (Sun et al. 2007). Also, the similar accumulation patterns of Cu and Zn in N. lugens may have resulted from the same ⫹2 charge. Alternatively, Cu, Zn, and Mo (in the lighter molar mass group) are essential elements for biological activities, but Cd and Pb (in the larger molar mass group) are nonessential elements. Previous works reported that different mechanisms were responsible for absorbing essential and nonessential elements in Chironomus (Timmermans et al. 1992). In Drosophila, Cu is often stored in the whole body, but Zn is stored in the front and back ends of the Malpighian tubule (SchoÞeld et al. 1997). In N. lugens, we found that Cu and Zn bioaccumulation patterns were similar, thereby suggesting that these elements may promote each otherÕs accumulation to some degree. Zn and Cu assimilated by N. lugens can be combined into different forms of metallothionein and then stored in different organs. It has been reported that Zn can effectively induce the metalloprotein that promotes Cu storage in insects (Niu et al. 2000), which may cause the synergetic effects of bioaccumulation between Cu and Zn in N. lugens. Comparisons of other stable elements in adult N. lugens will require further exploration. Cd and Pb were found to have antagonistic bioaccumulation mechanisms in N. lugens according to their load coefÞcients. Thus, combined contaminations of Cd and Pb may induce antagonistic effects on bioaccumulation mechanisms in adult N. lugens. This notion

660

ENVIRONMENTAL ENTOMOLOGY

is consistent with previous Þeld and laboratory studies on other insects. For example, in Galleria mellonella L., combined contamination (4 ␮g Pb/g with increasing concentrations of Cd) revealed antagonistic effects on the accumulation of Cd and Pb (Ortel 1995). Pb was accumulated to a lesser degree in the presence of Cd than in the absence of Cd, and vice versa. In Achaeta domestica (Gryllidae), less Pb and Cd were retained under combined exposure compared with single exposures (Migula et al. 1989). One study observed that, in chironomids, accumulations of three heavy metals (Cu, Cd, and Pb) were relatively decreased when they were exposed to a mixture of the three metals compared with when they were exposed to individual metal at similar concentrations. Furthermore, in chironomids, the antagonism between Cd and Pb may be because of the competition of the two metals for binding sites on the cell surface (Lagrana et al. 2011). In N. lugens, there may be the same situation that Cd and Pb have a competitive relationship for the same binding sites on the cell surface, so the bioaccumulation for the two metals have shown antagonistic effects. This study demonstrated that heavy metal bioaccumulation in N. lugens was related to the concentrations present in the rice plants they consumed. Our results suggest that the concentrations of Zn in N .lugens could be used as bioindicators of environmental contamination in rice paddy Þelds. The patterns of bioaccumulation of seven elements in N. lugens could be classiÞed into two groups according to their molar mass. The bioaccumulation mechanisms and interactions among these seven heavy metal elements require further exploration. Acknowledgments We thank De-Kang Duan, Guo-Guang Zhang, Hua Zhang, Jia-Xiang Zhuang, Shao-Dong Dang, Wei-bin Li, Xia-Rong Huang, You-An Yang, and Zai-Lin Liang for providing the samples of N. lugens, rice plants, and soils. This study was supported by the National Basic Research Program of China (Grant No. 2010CB126200), the National High Technology Research and Development Program (Grant No. 2006AA10Z217), and the National Special Funds for Meteorological ScientiÞc Research on Public Causes (Grant No.GYHY201006026).

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