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Entomotoxic efficacy of aluminium oxide, titanium dioxide and zinc oxide nanoparticles against Sitophilus oryzae (L.): A comparative analysis
Journal of Stored Products Research 83 (2019) 92e96
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Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Entomotoxic efficacy of aluminium oxide, titanium dioxide and zinc oxide nanoparticles against Sitophilus oryzae (L.): A comparative analysis Sumistha Das, Annu Yadav, Nitai Debnath* Amity Institute of Biotechnology, Amity University Haryana, Gurugram, 122413, India
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 March 2019 Received in revised form 29 May 2019 Accepted 8 June 2019
The development of resistance in both stored grain and field insect pests to conventional insecticides, coupled with increased consumer awareness of the consequences of their residual toxicity in food crops and environmental contamination have led agro-chemical researchers to reappraise the use of inert dusts as alternative insecticide. Diatomaceous Earth or DE became popular as an alternative insecticide in last two decades for its low mammalian toxicity and physical mode of action. But due to several limitations of DE many researchers are trying to explore the possibility of using nanoparticles as potential insecticide. In this study, a comparison on entomotoxic efficacy of different oxide nanoparticles like aluminium oxide, titanium dioxide and zinc oxide was evaluated on Sitophilus oryzae. Though more than 90% S. oryzae died after 4 days of nano aluminium oxide treatment at 1 g kg1 dosage, nano zinc oxide and titanium dioxide treatment could attain this efficacy at 2 g kg1 after 14 days. Even then use of nano zinc oxide and titanium dioxide in agriculture sector is preferred to nano aluminium oxide as the latter nanoparticle has adverse effects on plant growth. Moreover due to the antimicrobial property of nano zinc oxide and titanium dioxide have antimicrobial property, they will not only protect the agricultural produce from insect pests, but also from microbial infection. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Biosafety Diatomaceous earth Insect pest Nanocides Residual toxicity
1. Introduction Every year a huge volume of food reserve is wasted worldwide due to stored grain pest infestation. To feed the ever exploding human population a sustainable strategy should be adopted to control post harvest losses of stored grain crops. Stored grain insect pests mainly cause damage on food crop by direct feeding. A few insects feed on the endosperm causing physical and quality losses that reduce the economic value of the crop, while some other species feed on the germ resulting in poor seed germination and viability (Malek and Parveen, 1989; Santos et al., 1990). Moreover, stored food product becomes contaminated with insect pest excreta, molting, dead bodies and these ultimately cause secondary infection by bacteria and fungi. Among all insect orders coleopteran and lepidopteran insects cause the major post harvest crop damage (http://www.fao.org/3/a-av013e.pdf). Though the crop damage by lepidopteran insects is restricted to larval stage only, both adult and
* Corresponding author. E-mail address: [email protected] (N. Debnath). https://doi.org/10.1016/j.jspr.2019.06.003 0022-474X/© 2019 Elsevier Ltd. All rights reserved.
larval forms of Coleoptera are responsible for the same. Sitophilus oryzae or rice weevil is one of the primary stored grain pests. It is almost cosmopolitan in distribution throughout the tropical and sub tropical regions. Though it mainly feeds on rice, it can virtually grow on all types of cereals. The major strategy used to protect the crop storage is to apply chemical compounds, including both fumigants and contact insecticides. But these insecticides usually show toxicity to living organisms. Moreover, indiscriminate use of conventional insecticides causes environmental contamination and makes many an insect resistant to a number of insecticides including synthetic pyrethroids, organophosphates, carbamates, chlorinated hydrocarbons, Bacillus thuringiensis, botanicals and fumigants (Subramanyam and Hagstrum, 1995). In this context a newer strategy should be explored to combat all the drawbacks associated with the traditional insecticides. Nowadays pest management researchers are re-investigating the entomotoxic potential of inert dusts like diatomaceous earth (DE) (Subramanyam and Roesli, 2000; Mewis and Ulrichs, 2001), several formulations of which have become popular as alternative insecticide in last two decades (Athanassiou, 2008; Korunic, 2013; Akhtar and Isman, 2013; Ciesla and Guery, 2014; Adarkwah et al. 2018). But DE also
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has several limitations like it causes reduction in bulk density of the grain, its effectiveness depends on geographical origin, moisture content in the crop etc. (Vayias and Athanassiou, 2004). Now many researchers are also exploring the possibility of using nanoparticles (NPs) as potent insecticides (Debnath et al. 2010, 2011; 2012; Goswami et al. 2010; Stadler et al. 2010; Salem et al. 2015; pez-García et al. 2018; Keratum et al. 2015; Kitherian, 2017; Lo Padmasri et al. 2018). Though use of nanomaterials in agriculture has the potential to revolutionize this sector in several ways like controlling plants from plant pathogens (Elmer et al. 2018), reducing the dosage of agrochemicals by developing slow release formulations (Huang et al. 2018) etc., its application is still very much restricted in this arena. Nanoscale materials show many novel physico-chemical properties in comparison with their bulk counterpart. Specifically due to enhanced surface area to volume ratio NPs become more reactive and this is one of the reasons for which they may become insecticidal (Debnath et al. 2011). In this study a comparative entomotoxic efficacy of surface functionalized aluminium oxide NPs (ANPs), titanium dioxide NPs (TNPs) and zinc oxide NPs (ZNPs) was evaluated against S. oryzae. ANPs do not show significant toxicity against soil microorganisms (Fajardo et al. 2014) Wang et al. (2016) showed that TNPs are beneficial not only for plant germination and growth but also for crop disease control because of their antibacterial property. ZNPs are well known for their anti microbial property (Patra et al. 2012) and US FDA has enlisted ZnO as GRAS (generally recognized as safe) (Pulit-prociak et al. 2016).
2. Materials and methods 2.1. Nanoparticles Custom synthesized oxide NPs were procured from M K Implex, Canada. They were hydrophilic ANP-a and ANP-g, hydrophilic TNP (Anatase), hydrophilic and hydrophobic TNP (Rutile), hydrophilic, lipophilic and hydrophobic ZNP. Aluminium isopropoxide method (Park et al. 2005) was used for the production of ANP. ANP-a had size range of 35e45 nm (Fig. 1a), and ANP-g had size range of 13e20 nm (Fig. 1b). TNP, having size range of 45e60 nm (Fig. 1c, d, e), was made by the sol-gel method (Tao et al. 2008). ZNP was synthesized by the plasma vapor method (Chou Phillips, 1992) and had the size range of 50e350 nm (Fig. 1f, g, h). Micron sized aluminium oxide, titanium dioxide, zinc oxide were purchased from one Indian chemicals manufacturing company (Loba Chemie, India) to compare their insecticidal efficacy with their nano sized counterpart.
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2.2. Insects S. oryzae were reared on whole rice grain (IR64) at 30 C ± 1 C, 75 ± 5% R.H. in continuous darkness. Insects were inbred in the laboratory by sib-mating for 20 generations. The R.H. was maintained by using saturated solution of sodium chloride (Winston and Bates, 1960). Adults less than 2 weeks were used for the experiments. 2.3. Assessment of entomotoxic efficacy of surface functionalized aluminum oxide, titanium dioxide, zinc oxide nanoparticles Plastic screw capped boxes (diameter: 6 cm, height: 6.5 cm) with perforated caps were used for the insecticidal assay on S. oryzae. 20 g of rice (IR64), treated individually with the NPs at three dose rates - 0.5, 1 and 2 g nanoparticle kg1 rice was placed in each box. Same dosage of micron sized aluminium oxide; zinc oxide and titanium dioxide were also used in this bioassay. The boxes were shaken manually for approximately 1 min to achieve equal distribution of particles on rice (Subramanyam and Roesli, 2000). For each dose, there were five replicates. In one additional set no NP was mixed with rice and this set served as control. Then 20 adults of S. oryzae were introduced into each box. All bioassays were performed at 30 C ± 1 C, 75 ± 5% R.H. Insect mortality was checked after 1, 2, 4, 7 and 14 days. 2.4. Data analysis The data were analyzed by using a two-way ANOVA with R 2.14.2 software. Means were separated by using the Tukey-Kramer (HSD) test, at P ¼ 0.05. Control data were not included in the analysis, as control mortality was low (<10%). 3. Results All main effects and their associated interactions were significant at P < 0.01 (Table 1). Table 2 shows that at 2 g kg1 ANP-g was much more effective than other NPs after 1 day of treatment. On day 2, more than 90% insect mortality was obtained with ANP, when dosage rate was 2 g kg1. In fact at this dosage all the insects were killed in ANP-g treatment. Nearly 40% insects were dead when hydrophilic TNP (Anatase), hydrophobic TNP (Rutile) and lipophilic ZNP were applied at 2 g kg1 dosage (Table 3). After day 4, more than 90% S. oryzae died when ANP was applied at the dose of 1 g kg1. More than 45% of the insects died in the application of ZNP at 2 g kg1.60% insect mortality was obtained when hydrophilic TNP (Anatase) and hydrophobic TNP (Rutile) were applied at this dose (Table 4). After 7 days of exposure, both the ANPs could kill almost all the insects with 1 g kg1 dose (Table 5). In this time period hydrophobic TNP (Rutile) killed 93% insects at 2 g kg1 dose, whereas at this dose all ZNPs caused nearly 60% insect mortality. After 2 weeks, 60e75% mortality was found in all three types of ZNP and TNP at 1 g kg1. When the dosage was 2 g kg1 all TNPs and ZNPs caused more than 90% and more than 80% insect mortality respectively (Table 6). In all days nanomaterials were significantly more effective than their bulk size counter parts. No insect progeny was found in the rice stock even after 2 months of the experiment. 4. Discussion
Fig. 1. TEM image of hydrophilic (a) ANP- a and (b) ANP-g, SEM image of (c) hydrophilic TNP e Anatase, (d) hydrophilic TNP e Rutile, (e) TEM image of hydrophobic TNP e Rutile, SEM image of (f) hydrophilic ZNP, (g) hydrophobic ZNP and (h) lipophilic ZNP.
Many pest management researchers are actively involved in exploring the possibility of using inert dusts like DE as an alternative insecticide or acaricide (Athanassiou et al. 2004, 2006; 2007; Iatrou et al. 2010). But application of DE as insecticide has several
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Table 1 ANOVA parameters for main effects and their associated interactions. Source
Treatment Dose Treatment x dose
df
Day 1
10 2 20
Day 2
Day 3
Day 7
Day 14
F
P
F
P
F
P
F
P
F
P
64.81 123.13 27.73
<0.001 <0.001 <0.001
123.514 91.605 5.634
<0.001 <0.001 <0.001
210.362 107.651 7.163
<0.001 <0.001 <0.001
197.76 184.59 12.73
<0.001 <0.001 <0.001
217.7 221.6 13.1
<0.001 <0.001 <0.001
Table 2 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 1 day on rice treated with surface functionalized nanoparticles at 3 dose rates.
Table 5 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 7 days on rice treated with surface functionalized nanoparticles at 3 dose rates.
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
10 ± 6.12 Aa 8 ± 2.73 ABa 7 ± 2.73 Aa 4 ± 4.18 ABa 3 ± 2.73 ABa 3 ± 4.47 ABa 7 ± 2.73 Ba 1 ± 2.23 Ba 1 ± 2.23 Ba 1 ± 2.23 Ba 2 ± 4.47 BCa
18 ± 7.5 Aab 17 ± 5.7 ABa 16 ± 4.18 Aab 7 ± 7.58 BCa 2 ± 2.73 Ca 3 ± 2.73 Ca 16 ± 4.18 Ca 3 ± 4.7 Ca 1 ± 2.3 Ca 2 ± 2.73 Cab 4 ± 4.18 Ca
30 ± 10.6 Bb 89 ± 8.94 Ab 25 ± 3.53 Bb 5 ± 8.66 Ca 4 ± 6.51 Ca 27 ± 5.7 Bb 25 ± 3.53 Ca 6 ± 6.51 Ca 7 ± 4.47 Cb 7 ± 4.47 Cb 3 ± 4.47 Ca
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
72 ± 9.08 Ba 94 ± 6.51 Aa 24 ± 8.94 CDEa 27 ± 10.36 CDa 39 ± 4.18 Ca 16 ± 10.83 DEa 8 ± 2.73 Ea 40 ± 7.9 Ca 33 ± 8.36 Ca 33 ± 7.58 Ca 8 ± 5.7 Ea
100 Ab 97 ± 6.7 Aa 38 ± 7.58 BCb 45 ± 6.12 Bb 36 ± 9.61BCa 29 ± 6.51 Ca 8 ± 6.7 Da 47 ± 12.54 Ba 40 ± 5 BCa 36 ± 4.18 BCa 11 ± 4.18 Da
100 Ab 100 Aa 58 ± 5.7 Bc 65 ± 9.35 Bb 56 ± 9.61 Ba 93 ± 4.47 Ab 16 ± 2.23 Ca 59 ± 9.61 Ba 65 ± 12.74 Bb 62 ± 7.58 Bb 11 ± 6.51 Ca
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Table 3 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 2 days on rice treated with surface functionalized nanoparticles at 3 dose rates.
Table 6 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 14 days on rice treated with surface functionalized nanoparticles at 3 dose rates.
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
44 ± 10.8 ABb 57 ± 21.67 Aa 11 ± 4.18 CDa 14 ± 8.2 CDa 19 ± 6.51 CDa 8 ± 7.58 CDa 3 ± 4.47 Da 25 ± 6.12 BCa 16 ± 7.41 CDa 16 ± 6.51 CDa 2 ± 4.47 Da
63 ± 10.36 Bc 87 ± 7.58 Ab 22 ± 4.47 Cb 25 ± 6.12 Cb 18 ± 13.5 CDa 12 ± 7.58 CDa 5 ± 3.53 Da 28 ± 10.95 Ca 20 ± 6.2 CDa 17 ± 5.7 CDa 4 ± 4.18 Da
91 ± 10.83 Ad 100 Ab 32 ± 4.7 Bb 43 ± 10.36 Bc 20 ± 5 CDa 41 ± 8.94 Bb 6 ± 4.18 Da 32 ± 8.36 BCa 41 ± 8.94 Bb 36 ± 7.41 BCb 5 ± 6.12 Da
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
89 ± 9.61 Aa 100 Aa 31 ± 5.47 Ca 47 ± 10.36 Ba 51 ± 7.41 Ba 25 ± 7.07 CDa 10 ± 3.53 Da 62 ± 9.08 Ba 54 ± 10.83 Ba 54 ± 6.51 Ba 10 ± 3.53 Da
100 Ab 99 ± 2.23 Aa 44 ± 6.51 Cb 69 ± 9.61 Bb 58 ± 12.04 BCa 75 ± 10.6 Bb 12 ± 2.73 Da 74 ± 10.83 Bab 62 ± 6.7 Ba 62 ± 10.36 Ba 16 ± 4.18 Da
100 Ab 100 Aa 70 ± 5 Dc 94 ± 8.21ABCc 97 ± 4.47 ABb 99 ± 2.23 Ac 23 ± 4.47 Ab 83 ± 11.51 CDb 84 ± 6.51 BCb 82 ± 7.58 CDb 18 ± 6.7 Ea
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Table 4 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 4 days on rice treated with surface functionalized nanoparticles at 3 dose rates. Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
61 ± 6.51 Ba 94 ± 6.51 Aa 18 ± 7.58 CDEFa 23 ± 9.08 CDa 34 ± 7.41 Ca 13 ± 7.58 DEFa 6 ± 4.18 EFa 33 ± 11.51 Ca 27 ± 9.08 CDa 21 ± 5.47 CDEa 3 ± 4.47 Fa
91 ± 12.44 Ab 95 ± 6.12 Aa 30 ± 3.53 Bb 37 ± 8.36 Ba 29 ± 9.61 Ba 25 ± 10.6 Ba 6 ± 4.18 Ca 39 ± 8.94 Ba 30 ± 5 Ba 25 ± 5 Ba 7 ± 2.73 Ca
100 Ab 100 Aa 43 ± 5.7 CDc 60 ± 10 Bb 32 ± 8.36 Da 59 ± 6.51Bb 11 ± 4.18 Ea 46 ± 10.83 BDa 47 ± 9.08 BDb 51 ± 4.18 BCb 8 ± 7.58 Ea
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
limitations like its effectiveness depends on several factors like temperature (Kavallieratos et al. 2007; Vassilakos et al. 2006) R.H., geographical source (as silica and other mineral contents may vary
depending on the geographical location, Rojht et al. 2010). Nowadays nanotechnology shows considerable promise for use in agricultural sector starting from precision farming (Mfousavi and
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Rezaei, 2011), slow release to smart delivery of agrochemicals (Nurruzzaman et al. 2016). Nanosilica has been successfully used to control a broad range of insect pests (Debnath et al. 2009, 2010, 2011) in laboratory condition. In this study it was observed that all the nanomaterials irrespective of their surface functionalization were very much effective against S. oryzae. It was proposed by Ebeling and Wagner that insecticidal property of dusts gets increased if the particles are finer (Ebeling and Wagner, 1959). This was also evident from our experiments where it was observed that nanoparticulate forms of all oxide materials were much more effective than their micron sized counterparts. Because of their enormously increased exposed surfaces these NPs can more effectively interact with the protective cuticular wax layer of the insects. The insects get killed as their wax layer gets damaged due to both abrasion and adsorption of lipids and they start losing water from their body and ultimately die because of desiccation (Debnath et al. 2011). As the insecticidal effect of NPs are mostly physical in nature, there is probability that the insects are unlikely to become resistant to this mode of action very soon. Though in a previous study by Hamza et al. (2012) ZNP was found to impart 100% mortality on S. oryzae at 7th day, in this case ZNP and TNP were found to be reasonably toxic on 14th day at 2 g kg1. Rather in our bioassay ANP was found to be extremely effective in controlling rice weevil starting from day 4. Yet large scale use of ANP in agriculture is not much recommended as ANP in ground water inhibits the growth of carrot, cabbage, cucumber, corn and soybean (Yang and Watts, 2005). Moreover use of ZNP or TNP as insecticides has advantage over other conventional insecticides as these are potent anti microbial agents (Wang et al. 2016; Patra et al. 2012). Successful use of these nanomaterials will give protection not only against insect pests but also will prevent the agricultural produce from microbial infection. Moreover, zinc oxide and titanium dioxide are being used in cosmetics for years (Zvyagin et al. 2008; Newman et al. 2009) and this means that they are comparatively safe if human beings get exposed to these. Application of nano zinc oxide is also being increased even in biomedical field because of its less toxic property in comparison with other metallic NPs (Jiang et al. 2018). Many researchers studied the effect of ZNPs in agricultural crops like soybean, cucumber, cowpea (Vigna unguiculata), pearl millet (Pennisetum americanum), tomato etc. Though there was bioavailability of Zn in soybean pods, there was no accumulation of Zn in soybean grains (Hernandez-Viezcas et al. 2013). ZNPs did not have any impact on growth parameters of cucumber (Zhao et al. 2013), rather Tarfdar et al. (2014) reported that 15e25 nm sized ZNPs helped in promoting growth in pearl millet. Raliya et al. (2015) reported that both ZNP and TNP can promote plant growth up to a critical concentration. Moreover, TNPs are now being incorporated into fertilizers as they have the potential to increase crop yield by nitrogen photo reduction and photocatalytic bactericidal effect. Though it will be very premature to apply these nanocides in agricultural fields without going through extensive toxicity analysis, it can be used for protecting stored crops. These can be removed by conventional milling process unlike sprayable formulations of conventional insecticides. Therefore with proper safety measures ZNP and TNP can be used as stored grain as well as seed protecting agents. This study may lead to a new direction towards nanomaterial based insecticides for the agricultural sector. Acknowledgments Authors would like to thank Department of Biotechnology, Govt. of India, (DBT) (grant Nos e BT/PR9050/NNT/28/21/2007 & BT/ PR8931/NNT/28/07/2007) and Department of Science & Technology, Govt. of India, (DST) (grant No e YSS/2015/000152) for their financial support.
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Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Entomotoxic efficacy of aluminium oxide, titanium dioxide and zinc oxide nanoparticles against Sitophilus oryzae (L.): A comparative analysis Sumistha Das, Annu Yadav, Nitai Debnath* Amity Institute of Biotechnology, Amity University Haryana, Gurugram, 122413, India
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 March 2019 Received in revised form 29 May 2019 Accepted 8 June 2019
The development of resistance in both stored grain and field insect pests to conventional insecticides, coupled with increased consumer awareness of the consequences of their residual toxicity in food crops and environmental contamination have led agro-chemical researchers to reappraise the use of inert dusts as alternative insecticide. Diatomaceous Earth or DE became popular as an alternative insecticide in last two decades for its low mammalian toxicity and physical mode of action. But due to several limitations of DE many researchers are trying to explore the possibility of using nanoparticles as potential insecticide. In this study, a comparison on entomotoxic efficacy of different oxide nanoparticles like aluminium oxide, titanium dioxide and zinc oxide was evaluated on Sitophilus oryzae. Though more than 90% S. oryzae died after 4 days of nano aluminium oxide treatment at 1 g kg1 dosage, nano zinc oxide and titanium dioxide treatment could attain this efficacy at 2 g kg1 after 14 days. Even then use of nano zinc oxide and titanium dioxide in agriculture sector is preferred to nano aluminium oxide as the latter nanoparticle has adverse effects on plant growth. Moreover due to the antimicrobial property of nano zinc oxide and titanium dioxide have antimicrobial property, they will not only protect the agricultural produce from insect pests, but also from microbial infection. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Biosafety Diatomaceous earth Insect pest Nanocides Residual toxicity
1. Introduction Every year a huge volume of food reserve is wasted worldwide due to stored grain pest infestation. To feed the ever exploding human population a sustainable strategy should be adopted to control post harvest losses of stored grain crops. Stored grain insect pests mainly cause damage on food crop by direct feeding. A few insects feed on the endosperm causing physical and quality losses that reduce the economic value of the crop, while some other species feed on the germ resulting in poor seed germination and viability (Malek and Parveen, 1989; Santos et al., 1990). Moreover, stored food product becomes contaminated with insect pest excreta, molting, dead bodies and these ultimately cause secondary infection by bacteria and fungi. Among all insect orders coleopteran and lepidopteran insects cause the major post harvest crop damage (http://www.fao.org/3/a-av013e.pdf). Though the crop damage by lepidopteran insects is restricted to larval stage only, both adult and
* Corresponding author. E-mail address: [email protected] (N. Debnath). https://doi.org/10.1016/j.jspr.2019.06.003 0022-474X/© 2019 Elsevier Ltd. All rights reserved.
larval forms of Coleoptera are responsible for the same. Sitophilus oryzae or rice weevil is one of the primary stored grain pests. It is almost cosmopolitan in distribution throughout the tropical and sub tropical regions. Though it mainly feeds on rice, it can virtually grow on all types of cereals. The major strategy used to protect the crop storage is to apply chemical compounds, including both fumigants and contact insecticides. But these insecticides usually show toxicity to living organisms. Moreover, indiscriminate use of conventional insecticides causes environmental contamination and makes many an insect resistant to a number of insecticides including synthetic pyrethroids, organophosphates, carbamates, chlorinated hydrocarbons, Bacillus thuringiensis, botanicals and fumigants (Subramanyam and Hagstrum, 1995). In this context a newer strategy should be explored to combat all the drawbacks associated with the traditional insecticides. Nowadays pest management researchers are re-investigating the entomotoxic potential of inert dusts like diatomaceous earth (DE) (Subramanyam and Roesli, 2000; Mewis and Ulrichs, 2001), several formulations of which have become popular as alternative insecticide in last two decades (Athanassiou, 2008; Korunic, 2013; Akhtar and Isman, 2013; Ciesla and Guery, 2014; Adarkwah et al. 2018). But DE also
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has several limitations like it causes reduction in bulk density of the grain, its effectiveness depends on geographical origin, moisture content in the crop etc. (Vayias and Athanassiou, 2004). Now many researchers are also exploring the possibility of using nanoparticles (NPs) as potent insecticides (Debnath et al. 2010, 2011; 2012; Goswami et al. 2010; Stadler et al. 2010; Salem et al. 2015; pez-García et al. 2018; Keratum et al. 2015; Kitherian, 2017; Lo Padmasri et al. 2018). Though use of nanomaterials in agriculture has the potential to revolutionize this sector in several ways like controlling plants from plant pathogens (Elmer et al. 2018), reducing the dosage of agrochemicals by developing slow release formulations (Huang et al. 2018) etc., its application is still very much restricted in this arena. Nanoscale materials show many novel physico-chemical properties in comparison with their bulk counterpart. Specifically due to enhanced surface area to volume ratio NPs become more reactive and this is one of the reasons for which they may become insecticidal (Debnath et al. 2011). In this study a comparative entomotoxic efficacy of surface functionalized aluminium oxide NPs (ANPs), titanium dioxide NPs (TNPs) and zinc oxide NPs (ZNPs) was evaluated against S. oryzae. ANPs do not show significant toxicity against soil microorganisms (Fajardo et al. 2014) Wang et al. (2016) showed that TNPs are beneficial not only for plant germination and growth but also for crop disease control because of their antibacterial property. ZNPs are well known for their anti microbial property (Patra et al. 2012) and US FDA has enlisted ZnO as GRAS (generally recognized as safe) (Pulit-prociak et al. 2016).
2. Materials and methods 2.1. Nanoparticles Custom synthesized oxide NPs were procured from M K Implex, Canada. They were hydrophilic ANP-a and ANP-g, hydrophilic TNP (Anatase), hydrophilic and hydrophobic TNP (Rutile), hydrophilic, lipophilic and hydrophobic ZNP. Aluminium isopropoxide method (Park et al. 2005) was used for the production of ANP. ANP-a had size range of 35e45 nm (Fig. 1a), and ANP-g had size range of 13e20 nm (Fig. 1b). TNP, having size range of 45e60 nm (Fig. 1c, d, e), was made by the sol-gel method (Tao et al. 2008). ZNP was synthesized by the plasma vapor method (Chou Phillips, 1992) and had the size range of 50e350 nm (Fig. 1f, g, h). Micron sized aluminium oxide, titanium dioxide, zinc oxide were purchased from one Indian chemicals manufacturing company (Loba Chemie, India) to compare their insecticidal efficacy with their nano sized counterpart.
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2.2. Insects S. oryzae were reared on whole rice grain (IR64) at 30 C ± 1 C, 75 ± 5% R.H. in continuous darkness. Insects were inbred in the laboratory by sib-mating for 20 generations. The R.H. was maintained by using saturated solution of sodium chloride (Winston and Bates, 1960). Adults less than 2 weeks were used for the experiments. 2.3. Assessment of entomotoxic efficacy of surface functionalized aluminum oxide, titanium dioxide, zinc oxide nanoparticles Plastic screw capped boxes (diameter: 6 cm, height: 6.5 cm) with perforated caps were used for the insecticidal assay on S. oryzae. 20 g of rice (IR64), treated individually with the NPs at three dose rates - 0.5, 1 and 2 g nanoparticle kg1 rice was placed in each box. Same dosage of micron sized aluminium oxide; zinc oxide and titanium dioxide were also used in this bioassay. The boxes were shaken manually for approximately 1 min to achieve equal distribution of particles on rice (Subramanyam and Roesli, 2000). For each dose, there were five replicates. In one additional set no NP was mixed with rice and this set served as control. Then 20 adults of S. oryzae were introduced into each box. All bioassays were performed at 30 C ± 1 C, 75 ± 5% R.H. Insect mortality was checked after 1, 2, 4, 7 and 14 days. 2.4. Data analysis The data were analyzed by using a two-way ANOVA with R 2.14.2 software. Means were separated by using the Tukey-Kramer (HSD) test, at P ¼ 0.05. Control data were not included in the analysis, as control mortality was low (<10%). 3. Results All main effects and their associated interactions were significant at P < 0.01 (Table 1). Table 2 shows that at 2 g kg1 ANP-g was much more effective than other NPs after 1 day of treatment. On day 2, more than 90% insect mortality was obtained with ANP, when dosage rate was 2 g kg1. In fact at this dosage all the insects were killed in ANP-g treatment. Nearly 40% insects were dead when hydrophilic TNP (Anatase), hydrophobic TNP (Rutile) and lipophilic ZNP were applied at 2 g kg1 dosage (Table 3). After day 4, more than 90% S. oryzae died when ANP was applied at the dose of 1 g kg1. More than 45% of the insects died in the application of ZNP at 2 g kg1.60% insect mortality was obtained when hydrophilic TNP (Anatase) and hydrophobic TNP (Rutile) were applied at this dose (Table 4). After 7 days of exposure, both the ANPs could kill almost all the insects with 1 g kg1 dose (Table 5). In this time period hydrophobic TNP (Rutile) killed 93% insects at 2 g kg1 dose, whereas at this dose all ZNPs caused nearly 60% insect mortality. After 2 weeks, 60e75% mortality was found in all three types of ZNP and TNP at 1 g kg1. When the dosage was 2 g kg1 all TNPs and ZNPs caused more than 90% and more than 80% insect mortality respectively (Table 6). In all days nanomaterials were significantly more effective than their bulk size counter parts. No insect progeny was found in the rice stock even after 2 months of the experiment. 4. Discussion
Fig. 1. TEM image of hydrophilic (a) ANP- a and (b) ANP-g, SEM image of (c) hydrophilic TNP e Anatase, (d) hydrophilic TNP e Rutile, (e) TEM image of hydrophobic TNP e Rutile, SEM image of (f) hydrophilic ZNP, (g) hydrophobic ZNP and (h) lipophilic ZNP.
Many pest management researchers are actively involved in exploring the possibility of using inert dusts like DE as an alternative insecticide or acaricide (Athanassiou et al. 2004, 2006; 2007; Iatrou et al. 2010). But application of DE as insecticide has several
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S. Das et al. / Journal of Stored Products Research 83 (2019) 92e96
Table 1 ANOVA parameters for main effects and their associated interactions. Source
Treatment Dose Treatment x dose
df
Day 1
10 2 20
Day 2
Day 3
Day 7
Day 14
F
P
F
P
F
P
F
P
F
P
64.81 123.13 27.73
<0.001 <0.001 <0.001
123.514 91.605 5.634
<0.001 <0.001 <0.001
210.362 107.651 7.163
<0.001 <0.001 <0.001
197.76 184.59 12.73
<0.001 <0.001 <0.001
217.7 221.6 13.1
<0.001 <0.001 <0.001
Table 2 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 1 day on rice treated with surface functionalized nanoparticles at 3 dose rates.
Table 5 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 7 days on rice treated with surface functionalized nanoparticles at 3 dose rates.
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
10 ± 6.12 Aa 8 ± 2.73 ABa 7 ± 2.73 Aa 4 ± 4.18 ABa 3 ± 2.73 ABa 3 ± 4.47 ABa 7 ± 2.73 Ba 1 ± 2.23 Ba 1 ± 2.23 Ba 1 ± 2.23 Ba 2 ± 4.47 BCa
18 ± 7.5 Aab 17 ± 5.7 ABa 16 ± 4.18 Aab 7 ± 7.58 BCa 2 ± 2.73 Ca 3 ± 2.73 Ca 16 ± 4.18 Ca 3 ± 4.7 Ca 1 ± 2.3 Ca 2 ± 2.73 Cab 4 ± 4.18 Ca
30 ± 10.6 Bb 89 ± 8.94 Ab 25 ± 3.53 Bb 5 ± 8.66 Ca 4 ± 6.51 Ca 27 ± 5.7 Bb 25 ± 3.53 Ca 6 ± 6.51 Ca 7 ± 4.47 Cb 7 ± 4.47 Cb 3 ± 4.47 Ca
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
72 ± 9.08 Ba 94 ± 6.51 Aa 24 ± 8.94 CDEa 27 ± 10.36 CDa 39 ± 4.18 Ca 16 ± 10.83 DEa 8 ± 2.73 Ea 40 ± 7.9 Ca 33 ± 8.36 Ca 33 ± 7.58 Ca 8 ± 5.7 Ea
100 Ab 97 ± 6.7 Aa 38 ± 7.58 BCb 45 ± 6.12 Bb 36 ± 9.61BCa 29 ± 6.51 Ca 8 ± 6.7 Da 47 ± 12.54 Ba 40 ± 5 BCa 36 ± 4.18 BCa 11 ± 4.18 Da
100 Ab 100 Aa 58 ± 5.7 Bc 65 ± 9.35 Bb 56 ± 9.61 Ba 93 ± 4.47 Ab 16 ± 2.23 Ca 59 ± 9.61 Ba 65 ± 12.74 Bb 62 ± 7.58 Bb 11 ± 6.51 Ca
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Table 3 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 2 days on rice treated with surface functionalized nanoparticles at 3 dose rates.
Table 6 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 14 days on rice treated with surface functionalized nanoparticles at 3 dose rates.
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
44 ± 10.8 ABb 57 ± 21.67 Aa 11 ± 4.18 CDa 14 ± 8.2 CDa 19 ± 6.51 CDa 8 ± 7.58 CDa 3 ± 4.47 Da 25 ± 6.12 BCa 16 ± 7.41 CDa 16 ± 6.51 CDa 2 ± 4.47 Da
63 ± 10.36 Bc 87 ± 7.58 Ab 22 ± 4.47 Cb 25 ± 6.12 Cb 18 ± 13.5 CDa 12 ± 7.58 CDa 5 ± 3.53 Da 28 ± 10.95 Ca 20 ± 6.2 CDa 17 ± 5.7 CDa 4 ± 4.18 Da
91 ± 10.83 Ad 100 Ab 32 ± 4.7 Bb 43 ± 10.36 Bc 20 ± 5 CDa 41 ± 8.94 Bb 6 ± 4.18 Da 32 ± 8.36 BCa 41 ± 8.94 Bb 36 ± 7.41 BCb 5 ± 6.12 Da
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
89 ± 9.61 Aa 100 Aa 31 ± 5.47 Ca 47 ± 10.36 Ba 51 ± 7.41 Ba 25 ± 7.07 CDa 10 ± 3.53 Da 62 ± 9.08 Ba 54 ± 10.83 Ba 54 ± 6.51 Ba 10 ± 3.53 Da
100 Ab 99 ± 2.23 Aa 44 ± 6.51 Cb 69 ± 9.61 Bb 58 ± 12.04 BCa 75 ± 10.6 Bb 12 ± 2.73 Da 74 ± 10.83 Bab 62 ± 6.7 Ba 62 ± 10.36 Ba 16 ± 4.18 Da
100 Ab 100 Aa 70 ± 5 Dc 94 ± 8.21ABCc 97 ± 4.47 ABb 99 ± 2.23 Ac 23 ± 4.47 Ab 83 ± 11.51 CDb 84 ± 6.51 BCb 82 ± 7.58 CDb 18 ± 6.7 Ea
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
Table 4 Mean mortality (±S.E.) of Sitophilus oryzae adults exposed for 4 days on rice treated with surface functionalized nanoparticles at 3 dose rates. Nanoparticle
0.5 g kg1
1 g kg1
2 g kg1
Al2O3 (a) e hydrophilic Al2O3 (g) e hydrophilic Al2O3 e bulk TiO2 (Anatase) e hydrophilic TiO2 (Rutile) e hydrophilic TiO2 (Rutile) e hydrophobic TiO2 - bulk ZnO e hydrophilic ZnO e lipophilic ZnO e hydrophobic ZnO e bulk
61 ± 6.51 Ba 94 ± 6.51 Aa 18 ± 7.58 CDEFa 23 ± 9.08 CDa 34 ± 7.41 Ca 13 ± 7.58 DEFa 6 ± 4.18 EFa 33 ± 11.51 Ca 27 ± 9.08 CDa 21 ± 5.47 CDEa 3 ± 4.47 Fa
91 ± 12.44 Ab 95 ± 6.12 Aa 30 ± 3.53 Bb 37 ± 8.36 Ba 29 ± 9.61 Ba 25 ± 10.6 Ba 6 ± 4.18 Ca 39 ± 8.94 Ba 30 ± 5 Ba 25 ± 5 Ba 7 ± 2.73 Ca
100 Ab 100 Aa 43 ± 5.7 CDc 60 ± 10 Bb 32 ± 8.36 Da 59 ± 6.51Bb 11 ± 4.18 Ea 46 ± 10.83 BDa 47 ± 9.08 BDb 51 ± 4.18 BCb 8 ± 7.58 Ea
Within each column, means followed by the same upper case letter are not significantly different, within each row means followed by the same lower case letter are not significantly different; Tukey-Kramer HSD test; P ¼ 0.05.
limitations like its effectiveness depends on several factors like temperature (Kavallieratos et al. 2007; Vassilakos et al. 2006) R.H., geographical source (as silica and other mineral contents may vary
depending on the geographical location, Rojht et al. 2010). Nowadays nanotechnology shows considerable promise for use in agricultural sector starting from precision farming (Mfousavi and
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Rezaei, 2011), slow release to smart delivery of agrochemicals (Nurruzzaman et al. 2016). Nanosilica has been successfully used to control a broad range of insect pests (Debnath et al. 2009, 2010, 2011) in laboratory condition. In this study it was observed that all the nanomaterials irrespective of their surface functionalization were very much effective against S. oryzae. It was proposed by Ebeling and Wagner that insecticidal property of dusts gets increased if the particles are finer (Ebeling and Wagner, 1959). This was also evident from our experiments where it was observed that nanoparticulate forms of all oxide materials were much more effective than their micron sized counterparts. Because of their enormously increased exposed surfaces these NPs can more effectively interact with the protective cuticular wax layer of the insects. The insects get killed as their wax layer gets damaged due to both abrasion and adsorption of lipids and they start losing water from their body and ultimately die because of desiccation (Debnath et al. 2011). As the insecticidal effect of NPs are mostly physical in nature, there is probability that the insects are unlikely to become resistant to this mode of action very soon. Though in a previous study by Hamza et al. (2012) ZNP was found to impart 100% mortality on S. oryzae at 7th day, in this case ZNP and TNP were found to be reasonably toxic on 14th day at 2 g kg1. Rather in our bioassay ANP was found to be extremely effective in controlling rice weevil starting from day 4. Yet large scale use of ANP in agriculture is not much recommended as ANP in ground water inhibits the growth of carrot, cabbage, cucumber, corn and soybean (Yang and Watts, 2005). Moreover use of ZNP or TNP as insecticides has advantage over other conventional insecticides as these are potent anti microbial agents (Wang et al. 2016; Patra et al. 2012). Successful use of these nanomaterials will give protection not only against insect pests but also will prevent the agricultural produce from microbial infection. Moreover, zinc oxide and titanium dioxide are being used in cosmetics for years (Zvyagin et al. 2008; Newman et al. 2009) and this means that they are comparatively safe if human beings get exposed to these. Application of nano zinc oxide is also being increased even in biomedical field because of its less toxic property in comparison with other metallic NPs (Jiang et al. 2018). Many researchers studied the effect of ZNPs in agricultural crops like soybean, cucumber, cowpea (Vigna unguiculata), pearl millet (Pennisetum americanum), tomato etc. Though there was bioavailability of Zn in soybean pods, there was no accumulation of Zn in soybean grains (Hernandez-Viezcas et al. 2013). ZNPs did not have any impact on growth parameters of cucumber (Zhao et al. 2013), rather Tarfdar et al. (2014) reported that 15e25 nm sized ZNPs helped in promoting growth in pearl millet. Raliya et al. (2015) reported that both ZNP and TNP can promote plant growth up to a critical concentration. Moreover, TNPs are now being incorporated into fertilizers as they have the potential to increase crop yield by nitrogen photo reduction and photocatalytic bactericidal effect. Though it will be very premature to apply these nanocides in agricultural fields without going through extensive toxicity analysis, it can be used for protecting stored crops. These can be removed by conventional milling process unlike sprayable formulations of conventional insecticides. Therefore with proper safety measures ZNP and TNP can be used as stored grain as well as seed protecting agents. This study may lead to a new direction towards nanomaterial based insecticides for the agricultural sector. Acknowledgments Authors would like to thank Department of Biotechnology, Govt. of India, (DBT) (grant Nos e BT/PR9050/NNT/28/21/2007 & BT/ PR8931/NNT/28/07/2007) and Department of Science & Technology, Govt. of India, (DST) (grant No e YSS/2015/000152) for their financial support.
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