Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura

Physiological and Molecular Plant Pathology xxx (2017) 1e11

Contents lists available at ScienceDirect

Physiological and Molecular Plant Pathology journal homepage: www.elsevier.com/locate/pmpp

Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura Udaiyan Suresh a, Kadarkarai Murugan a, b, Chellasamy Panneerselvam c, Rajapandian Rajaganesh a, Mathath Roni a, Al Thabiani Aziz c, Hatem Ahmed Naji Al-Aoh d, Subrata Trivedi c, Hasibur Rehman c, Suresh Kumar e, Akon Higuchi f, Angelo Canale g, Giovanni Benelli g, * a

Division of Entomology, Department of Zoology, School of Life Sciences, Bharathiar University, Coimbatore, 641046, Tamil Nadu, India Thiruvalluvar University, Serkkadu, Vellore 632 115, Tamil Nadu, India c Biology Department, Faculty of Science, University of Tabuk, Tabuk, Saudi Arabia d Chemistry Department, Faculty of Science, University of Tabuk, Tabuk, Saudi Arabia e Department of Medical Microbiology and Parasitology, Universiti Putra Malaysia, 43400 Serdang, Slangor, Malaysia f Department of Chemical and Materials Engineering, National Central University, No. 300, Jhongda RD., Jhongli, Taoyuan, 32001 Taiwan g Department of Agriculture, Food and Environment, University of Pisa, Via Del Borghetto 80, 56124 Pisa, Italy b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 23 December 2016 Accepted 2 January 2017 Available online xxx

The overuse of synthetic pesticides to control insect pests leads to physiological resistance and adverse environmental effects, in addition to high operational cost. Insecticides of botanical origin have been reported as useful for control of agricultural and public health insect pests. This research proposed a novel method of mangrove-mediated synthesis of insecticidal silver nanoparticles (AgNP) using Suaeda maritima, acting as a reducing and stabilizing agent. AgNP were characterized by UVevis spectroscopy, Fourier transform infrared (FTIR) spectroscopy, scanning electron microscopy (SEM), energy-dispersive X-ray spectroscopy (EDX), and X-ray diffraction (XRD) analysis. S. maritima aqueous extract and mangrove-synthesized AgNP showed larvicidal and pupicidal toxicity against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura. In particular, LC50 of AgNP ranged from 8.668 (larva I) to 17.975 ppm (pupa) for A. aegypti, and from 20.937 (larva I) to 46.896 ppm (pupa) for S. litura. In the field, the application of S. maritima extract and AgNP (10
LC50) led to 100% mosquito larval reduction after 72 h. Smoke toxicity experiments conducted on A. aegypti adults showed that S. maritima leaf-, stem- and root-based coils evoked mortality rates comparable or higher if compared to permethrinbased positive control (62%, 52%, 42%, and 50.2 respectively). In ovicidal experiments, egg hatchability was reduced by 100% after treatment with 20 ppm of AgNP and 250 ppm of S. maritima extract. Furthermore, low doses of the AgNP inhibited the growth of Bacillus subtilis, Klebsiella pneumoniae and Salmonella typhi. Overall, our results highlighted the potential of S. maritima-based herbal coils and green nanoparticles as biopesticides in the fight against the dengue vector A. aegypti and the tobacco cutworm S. litura. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Arbovirus Crop protection Mangrove Antibacterial activity Nanotechnology

1. Introduction According to the report of FAO, US $120 billion losses worldwide

* Corresponding author. E-mail addresses: [email protected] (C. Panneerselvam), benelli.giovanni@ gmail.com (G. Benelli).

were caused by 20e40% decrease in crop yield, due to the attack from pathogenic organisms and insect pests [109]. Agriculture is the backbone of the Indian economy and nearly 75% of the rural areas of Indian villagers are depending on agriculture. The amount of food production is greatly deteriorated due to the crop pests and diseases, which lead to agricultural damage either directly by causing economic losses to the crops in the field or indirectly by

http://dx.doi.org/10.1016/j.pmpp.2017.01.002 0885-5765/© 2017 Elsevier Ltd. All rights reserved.

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

2

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

causing organoleptic alterations and/or the production of toxic substances [6]. The tobacco cutworm Spodoptera litura (Fab). (Lepidoptera: Noctuidae), is one of the major pests of many important crop plants. Since cutworm larvae can defoliate many economically important crops possessing a high dispersal capability, this pest often leads to high levels of agricultural losses [18,27]. This pest attacks more than 112 species of cultivated crops. Currently, large quantities of insecticides have been used to fight cutworm infestations on different crops [72]. Chemical pesticides play a significant role in increasing agricultural production by controlling the insect pests. Also, molecular research has revealed the interaction of autophagy-related protein 1 with autophagy-related protein 5 in S. litura [108]. However, there is widespread concern over negative impact of insecticides on environmental and human health due to accumulation of insecticide residues as well as emergence of pesticide resistance in the pests [5,9]. Due to this reason, many researchers focused on alternative control methods. Botanicals are effective against a variety of insect pests; they are easily degradable [15]. Besides crop pests, mosquitoes represent the major arthropod vectors of human disease worldwide, transmitting malaria, lymphatic filariasis, and arboviruses such as dengue fever and Zika virus [10,11,47,77]. Dengue, mainly vectored by the bites of infected Aedes mosquitoes, has the greatest epidemic potential worldwide, with huge negative impact on the economy and health of the population in urban areas [12e14]. Dengue can be divided into four serotypes (DENV 1, 2, 3, and 4), each of which confers partial crossprotective immunity to the other serotypes in humans [99]. Dengue is affecting more than 128 countries, and the results of biometric analysis of dengue burden in Arabian countries have been recently revealed [110]. Ever year about 390 million people are infected by dengue virus, among which 96 million become severe and results in about 21,000 deaths [16]. About half of the world's population is now at risk. The main transmission cycle is identified for dengue, which is largely caused by the urban adapted Aedes aegypti mosquitoes, and along with some other species such as Aedes albopictus [12,74]. Currently, a global alert has been issued for Zika, given the increase
syndrome, and other in congenital abnormalities, Guillain-Barre autoimmune manifestations, as well as the increase in chronic joint diseases due to chikungunya [62]. Since dengue and Zika virus are currently not vaccine preventable communicable diseases, vector control remains the only way to prevent arbovirus transmission [13,20,34]. As such, vector control and personal protection from the bites of infected mosquitoes are necessary [104]. Effective dengue control requires the community's participation. The community's health knowledge, attitudes and practices (KAP) will determine their participation in community-based programs. Taken together, these scenarios highlighted the need for effective and sustainable vector control strategies [9]. Very recently it is reported that a particular strain of Wolbachia can reduce the transmission of Zika virus by A. aegypti [2]. Overall, new drugs with unique structures and mechanisms of action are urgently required to treat drug-resistant strains of dengue [12]. Natural products and their derivatives from plants are continued to play an important role in the development of drugs for the treatment of human diseases as well as mosquitocides [64,112]. Mangroves are a rich source of biologically active and pharmacologically valuable natural products [40,80]. Therefore the present research presents recent advances in order to develop insecticidal compounds from mangrove plant extracts, with special reference to the green synthesis of silver nanoparticles. Mangrove forest ecosystems are characterized by facultative halophytic species of trees

and shrubs that fringe the intertidal zone along sheltered coastal, estuarine and riverine areas in tropical and subtropical latitudes [8,37]. Mangroves are biochemically unique vegetation that produces a wide array of natural products with immense medicinal potential [68,69]. They have been traditionally used in fisher-folk medicine to treat several diseases. It has been reported that the mostly halophytic genus Suaeda consists of 110 species worldwide covering the coastal areas of tropical and subtropical regions [29]. The distribution and zonation of different mangrove species also depends on physico-chemical variations of salinity and available nutrients [48,98]. Overall, mangroves have an immense ecological role in the coastal and marine environment [97]. Suaeda maritima (L.) Dumort (Chenopodiaceae) is a salt marshmangrove annual herb that grows in very alkaline and saline moist soils [78,80]. This plant is distributed throughout the east-west coast mangroves in India, i.e. Sunderbans in West Bengal, Mahnadhi and Bitharkanika in Orissa, Coringa, Krishna and Godavari in Andhra Pardesh, Karangadu and Pichavaram in Tamil Nadu. Leaf extracts of S. maritima have been used as traditional remedies for hepatitis [41], viral [61,71] and bacterial infections [45]. Nanotechnology is a promising field of interdisciplinary research. It opens up a wide array of opportunities in various fields including pest control, pharmaceuticals, electronics and parasitology [52e54,73]. Nowadays, the green synthesis of insecticidal nanoparticles is an interesting issue of nanoscience [11,25,46,57,75,77,81,84]. Synthesis of silver nanoparticles using mangroves scarcely analyzed the potential of nano-insecticides for insect pest management [58]. Therefore, in this research, a selected mangrove species (S. maritima) was used for biosynthesis of silver nanoparticles (AgNP) effective against insect pests of medical and agricultural relevance. S. maritima-fabricated AgNP were characterized by UVevis spectroscopy, Fourier transform infrared (FTIR) spectroscopy, scanning electron microscopy (SEM), energy-dispersive X-ray spectroscopy (EDX), and X-ray diffraction (XRD) analysis. We investigated the toxicity of the aqueous extract of S. maritima and S. maritima-synthesized AgNP in laboratory conditions against larvae and pupae of the dengue vector A. aegypti and the tobacco cutworm S. litura. We also evaluated the impact of S. maritima extract and AgNP as ovicides on A. aegypti. The smoke toxicity of herbal coils prepared using different parts of S. maritima on A. aegypti adults was studied. Both insecticides were validated in the field against A. aegypti. Finally, we also assessed antibacterial properties of AgNP against Bacillus subtilis, Klebsiella pneumoniae, and Salmonella typhi.

2. Materials and methods 2.1. Suaeda maritima collection and extraction S. maritima leaves were collected from coastal areas of Pichavaram (11250 47.900 N 79 480 08.500 E, Cuddalore district), Tamil Nadu, India. Specimens were washed with tap water and shade-dried at room temperature. Dried leaves were powdered using an electrical blender; 500 g of the powdered plant material were extracted using 1.5 L of ethanol for 72 h. The crude plant extract was concentrated at reduced temperature using a rotary evaporator, and stored at 22  C. One gram of the residue was dissolved in 100 mL of acetone (fixative agent to separate the aqueous impurities altering the chemical com-position of plant crude extract) and considered as 1% stock solution. From this stock solution, experimental concentrations were prepared [52,55].

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

2.2. Aedes aegypti and Spodoptera litura rearing A. aegypti were reared following the method by Suresh et al. and Murugan et al. [93,56] in laboratory conditions [27 ± 2  C, 75e85% R.H., 14:10 (L:D) photoperiod]. S. litura larvae were collected from the Central Institute of Cotton Research, Indian Council of Agricultural Research, Govt. of India, Coimbatore, India. They were cultured in laboratory and fed with Ricinius communis leaves ad libitum at 27 ± 2  C, 75e85% R.H., with 14:10 (L:D) photoperiod. Pre-pupae of S. litura were separated and provided with vermiculite clay, which is a good medium for pupation. Pupae of S. litura were kept on cotton in Petri dishes inside an adult emergence cage. The emerging moths were fed with 10% sucrose solution fortified with a few drops of vitamin mixture (MULTI DEC Vitamin drops) to enhance oviposition. Moths in the ratio of one male to one female were allowed inside oviposition cages containing the adult food mentioned above. The egg cage of S. litura was covered with white muslin cloth for egg laying. The egg clothes were removed daily and surface sterilized using 10% formaldehyde solution to prevent virus infection. The egg clothes were moistened and kept in a plastic container for the eggs to hatch. This process facilitated un-interrupted supply of test insects. 2.3. Biosynthesis and characterization of silver nanoparticles The S. maritima aqueous leaf extract was prepared adding 10 g of washed and finely cut leaves in a 300-ml Erlenmeyer flask filled with 100 ml of sterilized double distilled water and then boiling the mixture for 5 min, before finally decanting it. The extract was filtered using Whatman filter paper n. 1, stored at 4  C and tested within 5 days. The filtrate was treated with aqueous 1 mM AgNO3 solution in an Erlenmeyer flask and incubated at room temperature. A brown-yellow solution indicated the formation of AgNP, since aqueous silver ions were reduced by the S. maritima extract generating stable AgNP in water. Silver nitrate was purchased from the Precision Scientific Co. (Coimbatore, India). Green-synthesis of AgNP was confirmed by sampling the reaction mixture at regular intervals and the absorption maxima was scanned by UVevis, at the wavelength of 200e550 nm in UV-3600 Shimadzu spectrophotometer at 1 nm resolution. Furthermore, the reaction mixture was subjected to centrifugation at 15,000 rpm for 20 min, resulting pellet was dissolved in deionized water and filtered through Millipore filter (0.45 mm). An aliquot of this filtrate containing AgNP was used for scanning electron microscopy (SEM), Fourier transform infrared (FTIR) spectroscopy, X-ray diffraction (XRD) analysis, and energy dispersive X-ray (EDX) spectroscopy. The structure and composition of freeze-dried purified AgNP was analyzed by using a 10 kV ultra high-resolution scanning electron microscope with 25 ml of sample was sputter coated on copper stub and the images of AgNP were studied using a FEI QUANTA-200 SEM. The surface groups of the AgNP were qualitatively confirmed by FTIR spectroscopy (Stuart 2002), with spectra recorded by a Perkin-Elmer Spectrum 2000 FTIR spectrophotometer. EDX assays confirmed the presence of metals in analyzed samples [55,56]. 2.4. Mosquito larvicidal and pupicidal toxicity in laboratory conditions Twenty-five A. aegypti larvae (I, II, III or IV instar) or pupae were placed for 24 h in a glass beaker filled with 250 ml of dechlorinated water plus the desired concentration of S. maritima leaf extract (50, 100, 150, 200 and 250 ppm) or green-synthesized AgNP (5, 10, 15,

3

20 and 25 ppm). Larval food (0.5 mg) was provided for each tested concentration [39]. Each concentration was replicated five times against all instars. Control mosquitoes were exposed for 24 h to the corresponding concentration of the solvent. Percentage mortality was calculated as follows: Percentage mortality ¼ (number of dead individuals/number of treated individuals)*100

2.5. Mosquito field larvicidal assays Following the method by Suresh et al. [93]; the S. maritima leaf extract or AgNP were applied in six external water storage reservoirs at the National Institute of Communicable Disease Centre (Coimbatore, India), using a knapsack sprayer (Private Limited 2008, Ignition Products, India). Pre-treatment and posttreatment observations were conducted at 24, 48 and 72 h using a larval dipper. Toxicity was assessed against third- and fourth-instar larvae. Larvae were counted and identified to specific level. More than 90% of all surveyed larvae belong to A. aegypti. Six trials were conducted for each test site with similar weather conditions (28 ± 2  C; 80% R.H.). The required quantity of mosquitocidal was calculated on the basis of the total surface area and volume (0.25 m3 and 250 L); the required concentration was prepared using 10
LC50 values [51,93]. Percentage reduction of the larval density was calculated using the formula: Percentage reduction ¼ (C e T)/ C
100 where C is the total number of mosquitoes in the control and T is the total number of mosquitoes in the treatment. 2.6. Toxicity against the tobacco cutworm Spodoptera litura Toxicity against S. litura larvae and pupae was studied using the leaf disk assay with no-choice method. F2 generation larvae were fed with cotton leaf disks treated with different concentrations of S. maritima extract and mangrove-synthesized AgNP using the dipping method. After 24 h, the individuals were transferred to untreated fresh cotton leaves. The leaves were changed every 24 h. Mortality was recorded after 96 h of treatment. Five replicates were maintained for each treatment with 10 larvae per replicate (total, n ¼ 50). Percentage mortality was calculated using the following formula [36]: Corrected mortality ¼ (Mortality in treatment - mortality in control)/(100-mortality in control)*100. The survived larvae were fed with untreated cotton leaves until pupation. Pupal mortality was calculated by subtracting the number of emerging adults from the total number of pupae. 2.7. Smoke toxicity assays against Aedes aegypti Leaves of S. maritima were used to prepare herbal coils for smoke toxicity assays against A. aegypti. Coils were prepared as described by Suresh et al. [93]; using 4 g of powdered leaves, 2 g of sawdust (binding material) and 2 g of coconut shell charcoal powder (burning material). The three materials were mixed with distilled water forming a semi-solid paste. Mosquito coils (0.6 cm thickness) were prepared from the semi-solid paste and then dried in the shade. Negative control coils were prepared following the

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

4

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

same method, without adding S. maritima. Positive control was commercial permethrin-based coils [93]. Following [54], experiments were conducted in a glass chamber measuring 140 cm
120 cm
60 cm. A door measuring 60 cm
30 cm was situated at the front of the chamber. In each test, 100 adult female mosquitoes (age: five days old, blood-starved for three days) were released into the chamber and were provided with a 10% (w:v) sucrose solution. An immobilized pigeon with a shaven belly was tied inside the tightly closed chamber. Each pigeon was used only once. The experiment was repeated five times on five separate days for each treatment (i.e. S. maritima-based coil, positive and negative controls). All mosquitoes were exposed to the vapor of burning coils for 1 h. After each experiment, the number of fed and unfed (alive and dead) mosquitoes were counted. The protection provided by the smoke from the plant samples against biting A. aegypti was calculated in terms of percentage of unfed mosquitoes due to treatment: [(Number of unfed mosquitoes in treatment e Number of unfed mosquito in negative control) /Number of treated mosquitoes]
100

2.8. Mosquito ovicidal activity Following Su and Mulla [90] in ovicidal activity experiments, A. aegypti eggs were collected placing ovitraps (i.e. Petri dishes, diameter 60 mm, lined with filter paper and containing 100 ml of water) inside each cage. In A. aegypti assays, ovitraps were stored in the cages for 2 days from the blood meal of females. The eggs laid on filter paper lining were examined using a photomicroscope (Leica ES2, Germany). Then, the eggs were placed in a cage with six glass cups (diameter: 6 cm). Five of them were filled with water plus the S. maritima extract and AgNP treatments as follows: 50, 100, 150, 200 and 250 and 5, 10, 15, 20 and 25 ppm. The control cup was filled with distilled water. 100 eggs were placed in each cup. Five replicates were done for each dosage. After treatment, the eggs from each concentration were transferred to distilled water cups for hatching assessment after counting the eggs under microscope. The percent egg mortality was calculated on the basis of nonhatchability of eggs with unopened opercula [111]. The hatch rates were assessed 48 h post-treatment using the following formula [31]:

tested compounds, were inserted in each plate. Plates were incubated at 37  C for 24 h. After the incubation, the zone of inhibition was measured using a photomicroscope (Leica ES2, Germany). The zone of inhibition indicates the degree of sensitivity of bacteria to a given treatment; a bigger area of bacteria-free media surrounding an antibiotic disk means the bacteria are more sensitive to the compound(s) the disk contains [76]. 2.10. Data analysis SPSS software package 16.0 version was used for all analyses. For both insect species, acute toxicity data from laboratory assays and bacteria inhibition growth data were transformed into arcsine/ proportion values and then analyzed using a two-way ANOVA with two factors (i.e., dosage and mosquito instar or bacterium species). Means were separated by Tukey's HSD test. Furthermore, insect pest mortality data from laboratory assays were analyzed by probit analysis, calculating LC50 and LC90 following the method by Finney [28]. Mosquito larval density data from field assays were analyzed using a two-way ANOVA with two factors (i.e. the mosquitocidal treatment and the elapsed time from treatment). Means were separated using Tukey's HSD test (P < 0.05). In herbal coil toxicity experiment, the number of fed, unfed and dead mosquitoes were analyzed by a one-way ANOVA where the factor was the treatment (i.e. the coil). Means were separated using Tukey's HSD test (P < 0.05). Ovicidal data were transformed into arcsine√proportion values and analyzed by one-way ANOVA. Means were separated using Tukey's HSD test (P < 0.05). 3. Results and discussion 3.1. Characterization of S. maritima-fabricated silver nanoparticles The rapid synthesis of AgNPs was observed when the aqueous extract of S. maritima was incubated with the AgNO3 solution. The aqueous extract behaved as both reducing (from Agþ to Agо) as well as capping/stabilizing agent for nascent AgNPs. The rapid change of coloration indicated the formation of AgNPs. The absorption spectra of AgNPs at different time intervals showed highly symmetric absorption bands. A maximum absorption peak was observed at 340 nm (Fig. 1). The biosynthesis of AgNP can be confirmed by the formation of yellowish brown color, and this might be due to the excitation of the surface Plasmon vibration of

Egg mortality (%) ¼ (number of hatched larvae/total number of eggs)*100

2.9. Antibacterial activity S. maritima-synthesized AgNP were tested against B. subtilis, K. pneumoniae and S. typhi. All bacteria strains were provided by Microbial Type Culture, Collection and Gene Bank Institute of Microbial Technology, Sector 39-A, Chandigarh-160036 (India). For all species, bacterial cultures 18e24 h old were used for the preparation of testing cultures. All bacteria were grown in nutrient broth described by Dinesh et al. [22]. Each bacterial strain was inoculated and incubated at 37  C for 24 h. After this phase, the culture attained 2
106 cfu/mL, and was used for antibacterial assays. The antibacterial activity of S. maritima AgNP was assessed using the agar disk diffusion method [22]. The tested bacteria strains were swabbed on Muller-Hinton agar medium plates. Three sterilized filter paper disks, treated with three different concentrations of the

Fig. 1. UVevisualization of the absorption spectra of Suaeda maritima-synthesized Ag nanoparticles over different time intervals.

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

the synthesized AgNP [46]. Similarly Sangeetha et al. [82], reported AgNP synthesized using mangrove Excoecaria agallocha showed surface Plasmon absorbance bands at 434 nm. Furthermore Umashankari et al. [100], highlighted that the absorption spectrum of Rhizophora mucronata-synthesized AgNP showed an intense peak at 426 nm. XRD patterns showed intense peaks corresponding to (111), (200) and (220) Bragg's reflection based on the face-centered cubic structure of AgNP. Thus, XRD highlighted that AgNP formed by the reduction of AgNO3 with S. maritima leaf extract were crystalline in nature (Fig. 2) [70,85]. Furthermore Dubey et al. [24], reported the size of Ag nanocrystals as estimated from the full width at half maximum of the (111) peak of silver using the Scherrer formula was 20e60 nm. Additionally, the unassigned peaks were identified due to the presence of phytochemicals from extracts that may be capping on the surface of AgNP [87]. SEM studies shed light on size and morphological features of S. maritima-synthesized AgNP. S. maritima-synthesized AgNPs were predominantly spherical in shape (Fig. 3a). As regard to mangrovebased synthesis [58], showed Sonneratia alba-synthesized AgNP were mostly spherical and cubical in shape and showed a large distribution of sizes, with mean values of 20e60 nm. With reference to algae [57], reported that the SEM of Centroceras clavulatumsynthesized AgNP showed spherical and cubic structures with a size range of 35e65 nm. Furthermore, AgNPs fabricated using the seaweed frond extract of Caulerpa scalpelliformis were spherical in shape with an average size ranging from 20 to 35 nm [52] while Roni et al. [81] reported spherical AgNPs with size ranging from 40 to 65 nm fabricated with Hypnea musciformis extract. EDX revealed a strong signal in the Ag region, confirming the presence of elemental silver (Fig. 3b). Metallic silver nanocrystals showed a typical optical absorption peak approximately at 3 keV due to surface plasmon resonance [38,102]. EDX also showed the presence of oxygen, suggesting that AgNP were capped by the organic components present in the mangrove extract, as also highlighted by FTIR analyses [67]. FTIR studies were done in order to identify the possible biomolecules in S. maritima leaf extract, which may be responsible for synthesis and stabilization of AgNP (Fig. 4). The FTIR spectrum of S. maritima leaf extract-fabricated AgNP shows bands at 3525.57 cm1, 3290.34 cm1, 2944.38 cm1, 2831.64 cm1, 1718.49 cm1, 1647.87 cm1, 1407.42 cm1, 1113.32 cm1, 1020.24 cm1 and 596.33 cm1. The presence of peak at 3416 cm1 could be ascribed to OeH groups from polyphenols, proteins, enzymes and/or polysaccharides [94], while the peak at 2922 cm1 indicates carboxylic acid [43]. The strong intense peak at 1382 cm1 probably corresponds to CeN stretch vibrations, as well as to the

5

Fig. 3. (a) Scanning electron microscopy (SEM) micrograph showing the morphological characteristics of silver nanoparticles synthesized using the Suaeda maritima extract; (b) Energy dispersive X-ray (EDX) spectrum of silver nanoparticles synthesized using S. maritima.

amide I bands of proteins in the leaf extract [33]. The band at 1636.40 cm1 corresponds to C]O stretching of alcohols, amide I and nitro groups [83]. The peak obtained at 1019 cm1 is probably linked to the CeN stretching vibration of aliphatic amines, alcohols or phenols [105].

800

Intensity (cps)

600

3.2. Larvicidal and pupicidal toxicity on Aedes aegypti 400

200

0 20

40

60

80

2-theta (deg)

Fig. 2. X-ray diffraction pattern of Suaeda maritima-synthesized silver nanoparticles.

In laboratory assays, the leaf extract of S. maritima was moderately toxic to larval instars (I-IV) and pupae of Ae. aegypti, even if tested at low doses. with LC50 values ranging from 135 to 242 ppm (Table 1). Mortality was proportional to the tested dosage. Recent research has showed that different mangrove species can be a source of compounds with good mosquitocidal properties. For instance Yogananth et al. [107], reported that essential oil from Rhizophora mucronata mangrove leaves was highly toxic to IV instar larvae of An. stephensi and Cx. quinquefasciatus with LC50 values of

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

6

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

Fig. 4. Fourier transforms infrared (FTIR) spectrum of vacuum-dried S. maritima-synthesized silver nanoparticles.

Table 1 Acute toxicity of Suaeda maritima leaf extract against larvae and pupae of the dengue vector Aedes aegypti. Target

LC50 (LC90) (ppm)

95% confidence limit LC50 (LC90)

I instar II instar III instar IV instar Pupa

135.034 162.454 183.604 210.809 242.949

116.007 142.983 164.172 188.381 216.137

LCL (329.083) (380.995) (399.344) (436.988) (468.268)

Regression equation

c2 (df ¼ 4)

UCL (289.219) (327.934) (343.293) (370.755) (394.569)

152.403 183.844 208.032 243.539 286.328

(393.778) (473.007) (496.463) (556.311) (603.626)

y y y y y

¼ ¼ ¼ ¼ ¼

0.892 0.953 1.091 1.194 1.382

þ þ þ þ þ

0.007x 0.006x 0.006x 0.006x 0.006x

2.334 1.249 1.816 3.150 2.589

n.s. n.s. n.s. n.s. n.s.

LC50 ¼ lethal concentration that kills 50% of the exposed organisms. LC90 ¼ lethal concentration that kills 90% of the exposed organisms. c2 ¼ chi-square value. d.f. ¼ degrees of freedom. n.s. ¼ not significant (a ¼ 0.05).

0.051 mg/mL (An. stephensi) and 0.0514 mg/mL (Cx. quinquefasciatus) [56]. observed mortality in larvae and pupae of Ae. aegypti exposed to aqueous extract of the mangrove Bruguiera cilyndrica. Besides Balakrishnan et al. [7], studied the larvicidal activity of the marine actinobacteria, Streptomyces alboflavus from mangrove environment, which showed significant activity against Ae. aegypti (LC50 1.48) and An. stephensi (LC50 1.30). In addition Ravikumar et al. [80], noted that the mangrove extracts of B. cylindrica, Ceriops decandra, Lumnitzera racemosa, R. apiculata, and R. mucronata

exerted antiplasmodial activity against chloroquine-sensitive Plasmodium falciparum. As regards to the toxicity mechanisms, we have observed that the mangrove extract plus AgNPs can act as inhibitors of neurosecretory cells, leading to shirinkage of internal cuticle, and/or can act directly on epidermal cells responsible for the production of enzymes leading tanning and/or cuticular oxidation process [50,86]. S. maritima-synthesized AgNP were highly toxic against Ae. aegypti. LC50 ranged from 8 to 17 ppm (Table 2). To the best of our

Table 2 Acute toxicity of Suaeda maritima-synthesized silver nanoparticles against larvae and pupae of the dengue vector Aedes aegypti. Target

I instar II instar III instar IV instar Pupa

LC50 (LC90) (ppm)

8.668 (21.407) 10.102 (24.322) 12.239 (27.460) 14.893 (31.490) 17.975 (35.348)

95% confidence limit LC50 (LC90) LCL

UCL

0.909 (17.036) 8.386 (22.114) 10.648 (24.846) 13.354 (28.197) 16.386 (31.358)

12.302 11.512 13.645 16.429 19.846

Regression equation

(34.381) (27.476) (31.276) (36.482) (41.572)

y y y y y

¼ ¼ ¼ ¼ ¼

0.872 0.910 1.031 1.150 1.326

þ þ þ þ þ

0.101x 0.090x 0.084x 0.771x 0.074x

c2 (df ¼ 4)

9.487 5.178 1.946 2.906 4.248

n.s. n.s. n.s. n.s. n.s.

LC50 ¼ lethal concentration that kills 50% of the exposed organisms. LC90 ¼ lethal concentration that kills 90% of the exposed organisms. c2 ¼ chi-square value. d.f. ¼ degrees of freedom. n.s. ¼ not significant (a ¼ 0.05).

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

knowledge, this is the first report about the toxicity of S. maritimasynthesized nanoparticles against arthropods [58]. have reported that the Sonneratia alba-synthesized AgNPs were toxic against larvae and pupae of A. aegypti, LC50 values ranging from 3.15 ppm (I) to 13.61 ppm (pupa). Another study by Balakrishnan et al. [7] investigated that the larvicidal activity of AgNP synthesized using the leaf extract of Avicennia marina against Ae. aegypti and An. stephensi with LC50 values were 4.374 (An. stephensi) and 7.406 mg/ L (Ae. aegypti). Dinesh Kumar et al. [23] reported that the R. lamarckii-fabricated AgNP exhibit high HIV type 1 reverse transcriptase inhibitory activity with IC50 of 0.4 mg/ml. Gnanadesigan et al. [30] highlighted that the R. mucronata-fabricated AgNP tested against Ae. aegypti and Cx. quinquefasciatus had LC50 values ranging from 0.585 mg/L (Ae. aegypti) and 0.891 ppm (Cx. quinquefasciatus). In the field, the application of S. maritima leaf extract or AgNP (10
LC50) leads to the complete elimination of larval populations of A. aegypti after 72 h (Table 3). Field assays investigating mosquitocidal efficacy of green-synthesized AgNP are currently limited [22,91]. For example Suresh et al. [93], reported that the field application of P. niruri extract (10
LC50) lead to Ae. aegypti larval reduction of 39.9, 69.2, and 100%, after 24, 48, and 72 h, respectively. Rajaganesh et al. [77] highlighted a single application of Dicranopteris linearis fern extract in water storage reservoirs lead to 100% larval reduction of the dengue vector Ae. aegypti after 72 h. Also Panneerselvam et al. [65], reported that the leaf extract of Euphorbia hirta was highly effective in field trials against An. stephensi, as it led to larval density reductions of 13.17, 37.64 and 84.00% after 24, 48 and 72 h. The biotoxicity of these botanical preparations might be due to the thin oily layer of constituents with little polarity, which spread on the water surface cutting oxygen supply to mosquito larvae. In addition, a number of plant-borne compounds dissolve into the water and penetrate into the larvae through the respiratory tubes or cuticle, killing them by suffocation and/or poisoning [53,55,101]. For S. maritima-synthesized AgNP, we hypothesize that the high mortality rates exerted on Ae. aegypti may be due to the small size of AgNP, which allows them to pass through the insect cuticle and even into individual cells, where they interfere with molting and other physiological processes [10,44,66,91,92]. With reference to Sibased nanoformulates, it has been reported that the mode of action for insecticidal activity of nanosilica is through desiccation of insect cuticle by physicosorption of lipid and is also expected to cause damage in the cell membrane, resulting in cell lysis and death of the insects [96]; see also [81]. 3.3. Smoke toxicity of S. maritima-based coils Smoke toxicity experiments conducted on A. aegypti adults showed that S. maritima leaf-, stem- and root-based coils evoked mortality rates comparable or higher if compared to permethrinbased positive control (62%, 52%, 42%, and 50.2 respectively) (Table 4). In agreement with our experiments, after a single treatment with the leaf-, stem-, and root-based coils prepared using P. niruri, the percentages of unfed mosquitoes was 58%, 40%, and 61% [93]. [55] also highlighted the concrete potential to produce mosquitocidal coils against A. stephensi using the seaweed Ulva

7

lactuca as burning material. Furthermore, Vineetha and Murugan [103] reported that smoke toxicity effects of Aegle marmelos and Toddalia asiatica against Aedes aegypti. Haldar et al. [35], studied the effect of smoke toxicity of Ficus krishnae against An. stephensi and Cx. vishnui. The smoke toxicity against Aedes vectors is probably due to the presence of active compounds from the different plant parts, which are toxic for the central nervous system, producing the knockdown effect [1]. 3.4. Ovicidal activity In ovicidal experiments, egg hatchability of A. aegypti was reduced by 100% after treatment with 25 and 30 ppm of AgNP; the S. maritima extract exerted 100% mortality post-treatment with 250 ppm, while control eggs showed the 100% hatchability (Table 5). Currently, most botanical preparations, including nanoformulated ones, focused on larvicidal assays, while the ovicidal potential, which usually require higher doses to be effective, remains overlooked [10]. In this framework Rajaganesh et al. [77], pointed out the ovicidal activity of D. linearis-fabricated AgNP against Ae. aegypti, while Madhiyazhagan et al. [111] observed that the Sargassum muticum-synthesized AgNP was an effective oviposition deterrent against An. stephensi, Ae. aegypti and Cx. quinquefasciatus at 50 ppm. Later on, Chandramohan et al. [19] have reported that the ovicidal properties Acorus calamus-synthesized AgNP on the malaria vector Anopheles stephensi. Concerning plant extracts, Cocculus hirsutus methanol extract caused 86% and 100% ovicidal activity against An. subpictus when tested at 500 ppm and 1000 ppm [26], while Govindarajan and Rajeswary [32] observed that the methanolic leaf extract of Albizia lebbeck exerted zero hatchability on Cx. quinquefasciatus, Ae. aegypti, and An. stephensi at 250, 200, and 150 ppm, respectively. Recently Munusamy et al. [49], showed that the methanol extract of Rubia cordifolia root had good ovicidal activity (82.40% and 70.40%) against the eggs of Cx. quinquefasciatus and Ae. aegypti, at 500 mg/L when compared to other plants, such as Gymnema sylvestre, Scilla peruviana, S. cordifolia and Elytraria acaulis (see also [4,64]. 3.5. Toxicity against the tobacco cutworm Spodoptera litura The S. maritima leaf extract was moderately toxic to larvae and pupae of Spodoptera litura. LC50 ranged from 268 to 609 ppm (Table 6). To the best of our knowledge, studies on mangrove-based biopesticides and related compounds against agricultural pests, with special reference to the tobacco cutworm, are scarce. Rani et al. [79] studied antifeedant and toxic activity of Hibiscus tiliaceus and Sonneratia caseolaris on S. litura. Furthermore Deshmukhe et al. [21], reported that the aqueous crude extract of Lantana camara leaves achieved 100% mortality on fourth instar larvae of S. litura when tested at 40%. Ananthi and Ranjitha Kumari [3] studied that the larvicidal activity of seed and root extract of Rorippa indica against S. litura. In addition to acute toxicity, a long term mortality effect evoked by mangrove extract on S. litura larvae may be due the active plant compounds entering into the body of the larvae and suppressing the activity of ecdysone, thus larva fails to molt, leading to disruption of normal physiological and metabolic

Table 3 Field reduction of Aedes aegypti larval populations post-treatment with Suaeda maritima leaf extract and green-synthesized silver nanoparticles in water storage reservoirs. Suaeda maritima extract (10xLD50) Before treatment Larval density

a

122.60 ± 8.32

Green-synthesized Ag nanoparticles (10xLD50)

24 h 85.60 ± 5.45

48 h b

51.20 ± 8.67

72 h cd

Before treatment e

0.00 ± 0.00

a

135.40 ± 6.76

24 h 59.00 ± 8.63

48 h c

72 h d

37.80 ± 6.14

0.00 ± 0.00e

Means ± SD followed by different letter(s) are significantly different (ANOVA, Tukey's HSD test, P < 0.05).

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

8

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11

Table 4 Smoke toxicity assays conducted using Suaeda maritima-based coils against the biting activity of the dengue vector Aedes aegypti. Treatment

Fed mosquitoes (%)

Unfed mosquitoes (%)

Total (%)

Alive 14.4 ± 1.67b 21.8 ± 0.83c 28.4 ± 1.14d 75.2 ± 1.48e 10.20 ± 1.30a

Leaf-based coil Stem-based coil Root-based coil Negative control (blank coil) Positive control (pyrethrin-based coil)

24.6 28.4 31.6 25.0 40.6

Dead

± ± ± ± ±

2.40a 1.67ab 1.34b 1.58a 1.67c

62.00 ± 2.12d 51.8 ± 1.09c 41.6 ± 1.51b 0.0 ± 0.0a 50.2 ± 1.48c

86.6 79.8 72.2 25.0 90.2

± ± ± ± ±

0.54d 1.92c 0.83b 1.22a 1.92d

Within each column, different letters indicate significant differences (ANOVA, Tukey's HSD, P < 0.05).

Table 5 Ovicidal activity of Suaeda maritima leaf extract and Suaeda maritima-synthesized silver nanoparticles on Aedes aegypti. Treatment

Egg hatchability (%) Control

Suaeda maritima extract Ag nanoparticles

86.2.83 ± 0.83 Control 91.20 ± 0.83a

50 ppm a

100 ppm b

61.40 ± 1.14 5 ppm 53.00 ± 1.58b

150 ppm

41.80 ± 1.30 10 ppm 36.6 ± 1.14c

c

200 ppm

29.20 ± 0.83 15 ppm 25.2 ± 1.30d

d

250 ppm e

21.2 ± 1.30 20 ppm NH

NH 25 ppm NH

Values were means ± SD of 5 replicates. Within a row, different letters indicated significant differences (ANOVA, TUkey's HSD, P < 0.05). NH ¼ no hatchability.

processes [59]. The S. maritima-synthesized AgNP were more effective than the mangrove extract alone on S. litura. LC50 ranged from 20 to 46 ppm (Table 7). To the best of our knowledge, most toxicity studies on green synthesized nanoparticles focused on pests of medical and veterinary importance (mainly mosquitoes and ticks), while efforts

on crop pests are rather rare. Durga Devi et al. [25] reported that the E. hirta-fabricated AgNP showed good insecticidal properties against Helicoverpa armigera, with LC50 values ranging from 2.905 ppm (I) to 3.086 ppm (pupa). Furthermore, Roni et al. [81], highlighted H. musciformis-synthesized AgNP were highly toxic against P. xylostella, LC50 were 24.51 ppm (I), 26.47 ppm (II),

Table 6 Acute toxicity of Suaeda maritima leaf extract on larvae and pupae of Spodoptera litura. Target

LC50 (LC90) (ppm)

95% confidence limit LC50 (LC90) LCL

I instar II instar III instar IV instar V instar VI instar Pupa

268.784 310.383 348.772 393.165 448.269 530.823 609.045

(631.237) (696.523) (757.492) (815.147) (874.430) (945.397) (992.761)

233.137 275.329 312.319 353.620 402.646 473.002 537.923

Regression equation

c2 (df ¼ 4)

UCL (560.088) (611.553) (657.766) (701.541) (746.680) (801.036) (836.771)

301.371 346.622 391.528 445.957 516.636 626.767 734.968

(742.857) (834.415) (925.063) (1011.14) (1100.09) (1207.19) (1284.33)

y y y y y y y

¼ ¼ ¼ ¼ ¼ ¼ ¼

0.950 1.030 1.094 1.194 1.348 1.641 2.034

þ þ þ þ þ þ þ

0.004x 0.003x 0.003x 0.003x 0.003x 0.003x 0.003x

0.171 0.018 0.077 0.150 0.375 0.172 0.408

n.s. n.s. n.s. n.s. n.s. n.s. n.s.

LC50 ¼ lethal concentration that kills 50% of the exposed organisms. LC90 ¼ lethal concentration that kills 90% of the exposed organisms. c2 ¼ chi-square value. d.f. ¼ degrees of freedom. n.s. ¼ not significant (a ¼ 0.05).

Table 7 Acute toxicity of Suaeda maritima-synthesized silver nanoparticles on larvae and pupae of Spodoptera litura. Target

LC50 (LC90) (ppm)

95% confidence limit LC50 (LC90)

I instar II instar III instar IV instar V instar VI instar Pupa

20.937 23.936 26.981 31.798 35.961 39.238 46.896

17.438 20.659 23.558 28.586 32.561 35.597 42.440

LCL (50.663) (54.790) (61.987) (67.300) (73.483) (77.648) (85.347)

Regression equation

c2 (df ¼ 4)

UCL (45.907) (49.496) (55.216) (59.713) (64.526) (67.771) (73.825)

23.824 26.792 30.140 35.193 40.020 43.965 53.521

(57.557) (62.566) (72.455) (79.158) (87.956) (93.901) (104.862)

y y y y y y y

¼ ¼ ¼ ¼ ¼ ¼ ¼

0.903 0.994 0.988 1.148 1.228 1.309 1.563

þ þ þ þ þ þ þ

0.043x 0.042x 0.037x 0.036x 1.034x 0.033x 0.33x

4.094 3.770 1.672 1.706 1.900 1.550 0.558

n.s. n.s. n.s. n.s. n.s. n.s. n.s.

LC50 ¼ lethal concentration that kills 50% of the exposed organisms. LC90 ¼ lethal concentration that kills 90% of the exposed organisms. c2 ¼ chi-square value. d.f. ¼ degrees of freedom. n.s. ¼ not significant (a ¼ 0.05).

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11 Table 8 Zone of inhibition induced by Suaeda maritima-synthesized silver nanoparticles on the bacteria B. subtilis, K. pneumoniae and S. typhi. Species

Inhibition zone (mm) Control

B. subtilis K. pneumoniae S. typhi

30 ppm a

8.16 ± 0.15 9.03 ± 0.05a 9.83 ± 0.15a

60 ppm b

16.10 ± 0.10 14.20 ± 0.17b 12.06 ± 0.11b

90 ppm c

20.16 ± 0.15 17.03 ± 0.05c 18.13 ± 0.11c

23.10 ± 0.10d 21.1 ± 0.20d 20.0 ± 0.03d

Values are means ± standard deviation of 3 replicates. Within a row, different letters indicate significant differences (ANOVA, Tukey's HSD, P < 0.05).

28.35 ppm (III), 32.55 ppm (IV) and 38.23 ppm (pupa). Yasur and Usha Rani [106] studied the impact of AgNP on growth and feeding responses of two lepidopteran pests, S. litura and Achaea janata. The insecticidal properties of green fabricated nanoparticles are mainly due to their morphological features, in particular their optical properties coupled with the high surface:volume ratio, that allow a boosted delivery of toxic bioactive compounds from plants, leading to key physiological changes [60]; it is worthy to note that their use is new in the field of agricultural pest management [10e13,17]. 3.6. Antibacterial activity In our experiments, S. maritima-synthesized AgNPs showed good antibacterial properties against B. subtilis, K. pneumoniae, and S. typhi (Table 8). At the maximum concentration tested (90 ppm), AgNP showed strong inhibitory action against B. subtilis (zone of inhibition 23.10 mm), K. pneumoniae (zone of inhibition 21.1 mm) and S. typhi (zone of inhibition 20.0 mm) (Table 8). Currently, green synthesized nanoparticles have been extensively surveyed against microbial pathogens. As a recent example related to mangroves [58], showed the good antibacterial activity of S. alba-synthesized AgNPs against B. subtilis, K. pneumoniae, and S. typhi. Furthermore Thatoi et al. [95], reported that the Heritiera fomes and S. apetalasynthesized AgNP showed high antibacterial potential than the ZnO NP against Staphylococcus aureus, Shigella flexneri, Vibrio cholera, Staphylococcus epidermidis, Bacillus subtilis, and Escherichia coli. Panja et al. [63]. reported that the antimicrobial activity of Rauvolfia serpentina-fabricated AgNP was high on B. subtilis, Enterococcus faecalis, Pseudomonas aeruginosa, and E. coli, using disk methods. In addition, Mahyoub et al. [46] highlighted that AgNP fabricated using Halodule uninervis showed good antibacterial activity against B. subtilis, K. pneumoniae and S. typhi. The exact mechanism for the antibacterial activity of AgNPs is not fully clarified. However, many studies report that the AgNP could bind to the bacterial membrane, invade the cell and cause appetite of proton motive force which leads to the distruction of bacterial cell by forming pores on the cell wall. Secondly, AgNP can interfere with the thiol group of bacterial cells leading to ceasure of respiratory chain reaction, cell division and death [89]. 4. Conclusions We have reported an easy, simple, and environmentally friendly approach for the synthesis of AgNP mediated by mangrove leaf extract of S. maritima as a reducing and capping/stabilizing agent. UVeVis spectrophotometry, XRD analysis, SEM, EDX spectroscopy, and FTIR spectroscopy confirmed the rapid and cheap synthesis of AgNP. Our results pointed out that S. maritima and seaweedsynthesized AgNP toxic against invertebrates of medical and agricultural importance, including dengue mosquitoes and the tobacco cutworm, allowing us to propose the tested products as effective candidates to develop newer and safer botanical insecticides. We

9

also noted that relatively low doses of green-synthesized AgNP effectively inhibit several species of microbial pathogens [46]. Further studies are in progress to optimize this synthesis route, evaluating the toxicity of intermediate reaction products on different insect pests of economic relevance. References [1] D. Abirami, K. Murugan, HPTLC quantification of flavonoids, larvicidal and smoke repellent activities of Cassia occidentalis L. (Caesalpiniaceae) against malarial vector Anopheles stephensi Lis (Diptera: Culicidae), J. Phytol. 3 (2) (2011) 60e72. [2] M.T. Aliota, S.A. Peinado, I.D. Velez, J.E. Osorio, The wmel strain of wolbachia reduces transmission of zika virus by Aedes aegypti, Sci. Rep. 6 (2016) 28792. [3] P. Ananthi, B.D. Ranjithakumari, Larvicidal activity of Rorippa indica L. against Spodoptera litura Fab, Eur. J. Exp. Biol. 6 (3) (2016) 68e74. [4] D.R. Appadurai, M. Rajiv Gandhi, M.G. Paulraj, S. Ignacimuthu, Ovicidal and oviposition deterrent activities of medicinal plant extracts against Aedes aegypti L. and Culex quinquefasciatus say mosquitoes (Diptera: Culicidae), Osong Public Health Res. Perspect. 6 (1) (2015) 64e69. [5] N.J. Armes, J.A. Wightman, D.R. Jadhav, G.V.R. Rao, Status of insecticide resistance in Spodoptera litura in Andhra Pradesh, India, Pest Sci. 50 (1997) 240e248. [6] E. Arumugam, B. Muthusamy, K. Dhamodaran, M. Thangarasu, K. Kaliyamoorthy, E. Kuppusamy, Pesticidal activity of Rivina humilis L. (Phytolaccaceae) against important agricultural polyphagous field pest, Spodoptera litura (Fab.) (Lepidoptera: noctuidae), J. Coast Lif Med. 3 (5) (2015) 389e394. [7] S. Balakrishnan, M. Srinivasan, J. Mohanraj, Biosynthesis of silver nanoparticles from mangrove plant (Avicennia marina) extract and their potential mosquito larvicidal property, J. Parasit. Dis. 40 (2016) 991e996. [8] W.M. Bandaranayake, Bioactivities bioactive compounds and chemical constituents of mangrove plants, Wet. Eco Manag. 10 (2002) 421e452. [9] G. Benelli, Research in mosquito control: current challenges for a brighter future, Parasitol. Res. 114 (2015) 2801e2805. [10] G. Benelli, Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review, Parasitol. Res. 115 (2016a) 23e34. [11] G. Benelli, Plant-mediated synthesis of nanoparticles: a newer and safer tool against mosquito-borne diseases? Asia Pacif. J. Trop. Biomed. 6 (2016b) 353e354. [12] G. Benelli, Green synthesized nanoparticles in the fight against mosquitoborne diseases and cancer - a brief review, Enzym Microb. Technol. 95 (2016c) 58e68. [13] G. Benelli, Spread of Zika virus: the key role of mosquito vector control, Asia Pac. J. Trop. Biomed. 6 (2016d) 468e471. [14] G. Benelli, H. Mehlhorn, Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control, Parasitol. Res. 115 (2016) 1747e1754. [15] G. Benelli, R. Pavela, F. Maggi, R. Petrelli, M. Nicoletti, Commentary: making green pesticides greener? The potential of plant products for nanosynthesis and pest control, J. Clust. Sci. (2017), http://dx.doi.org/10.1007/s10876-0161131-7. [16] S. Bhatt, P.W. Gething, O.J. Brady, J.P. Messina, A.W. Farlow, C.L. Moyes, J.M. Drake, J.S. Brownstein, A.G. Hoen, O. Sankoh, M.F. Myers, D.B. George, T. Jaenisch, G.R. William Wint, C.P. Simmons, T.W. Scott, J.J. Farrar, S.I. Hay, The global distribution and burden of dengue, Nature 496 (2013) 504e507. [17] A. Bhattacharyya, A. Bhaumik, R.P. Usha, S. Mandal, T.T. Epidi, Nano particles a recent approach to insect pest control, Afr. J. Biotechnol. 9 (2010) 3489e3493. [18] A. Bhattacharyya, S. Mazumdar Leighton, C.R. Babu, Bioinsecticidal activity of Archidendron ellipticum trypsin inhibitor on growth and serine digestive enzymes during larval development of Spodoptera litura, Comp. Biochem. Physiol. 145 (2007) 669e677. [19] B. Chandramohan, K. Murugan, K. Kovendan, C. Panneerselvam, P. Mahesh Kumar, P. Madhiyazhagan, D. Dinesh, U. Suresh, J. Subramaniam, D. Amaresan, T. Nataraj, D. Nataraj, J.S. Hwang, A.A. Alarfaj, M. Nicoletti, A. Canale, H. Mehlhorn, G. Benelli, Do nanomosquitocides impact predation of Mesocyclops edax copepods against Anopheles stephensi larvae?, in: H. Mehlhorn (Ed.), Nanoparticles in the Fight against Parasites. Parasitol Res Monogr, Springer ISSN, 2015, pp. 2192e3671. [20] J.L. Deen, The challenge of dengue vaccine development and introduction, Trop. Med. Int. Health 9 (1) (2004) 1e3. [21] P.V. Deshmukhe, A.A. Hooli, S.N. Holihosur, Effect of Lantana camara (L.) on growth, development and survival of tobacco caterpillar (Spodoptera litura Fabricius), Karnat. J. Agric. Sci. 24 (2) (2011) 137e139. [22] D. Dinesh, K. Murugan, P. Madhiyazhagan, C. Panneerselvam, M. Nicoletti, J.S. Hwang, G. Benelli, B. Chandramohan, U. Suresh, Mosquitocidal and antibacterial activity of green-synthesized silver nanoparticles from Aloe Vera extracts: towards an effective tool against the malaria vector Anopheles stephensi? Parasitol. Res. 114 (2015) 1519e1529. [23] Dinesh Kumar, G. Singaravelu, S. Ajithkumar, K. Murugan, M. Nicoletti, G. Benelli, Mangrove-mediated green synthesis of silver nanoparticles with

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

10

[24]

[25]

[26]

[27]

[28] [29] [30]

[31]

[32]

[33]

[34] [35]

[36]

[37] [38]

[39]

[40]

[41]

[43]

[44]

[45]

[46]

[47] [48]

[49]

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11 high HIV-1 reverse transcriptase inhibitory potential, J. Clust. Sci. (2016), http://dx.doi.org/10.1007/s10876-016-1100-1. M. Dubey, S. Bhadauria, B.S. Kushwah, Green synthesis of nanosilver particles from extract of Eucalyptus Hybrida (Safeda) leaf, Dig. J. Nanomater Biostruct. 4 (3) (2009) 537e543. G. Durga Devi, K. Murugan, C. Panneerselvam, Green synthesis of silver nanoparticles using Euphorbia hirta (Euphorbiaceae) leaf extract against crop pest of cotton bollworm, Helicoverpa armigera (Lepidoptera: noctuidae), J. Biopest. 7 (2014) 54e66. G. Elango, A. Bagavan, C. Kamaraj, A. AbduzZahir, A. Abdul Rahuman, Oviposition-deterrent, ovicidal, and repellent activities of indigenous plant extracts against Anopheles subpictus Grassi (Diptera: Culicidae), Parasitol. Res. 105 (6) (2009) 1567e1576. K. Elumalai, K. Krishnappa, A. Anandan, M. Govindarajan, T. Mathivanan, Certain essential oil against the field pest army worm, Spodoptera litura (lepidoptera:noctuidae), Inter J. Rec. Sci. Res. 2 (2010) 056e062. D.J. Finney, Probit Analysis, Cambridge University, London, 1971, pp. 68e78. Z. Gelin, S.L. Mosyakin, S.E. Clemants, Chenopodiaceae, Flor. Chin. 5 (2003) 351e414. M. Gnanadesigan, M. Anand, S. Ravikumar, M. Maruthupandy, V. Vijayakumar, S. Selvam, M. Dhineshkumar, A.K. Kumaraguru, Biosynthesis of silver nanoparticles by using mangrove plant extract and their potential mosquito larvicidal property, Asia Pac. J. Trop. Med. (2011) 799e803. M. Govindarajan, T. Mathivanan, K. Elumalai, K. Krishnappa, A. Anandan, Ovicidal and repellent activity of botanical extracts against Culex quinquefasiatus, Aedes aegypti and Anopheles stephensi, (Diptera: Culicidae), Asia Pac. J. Trop. Med. 1 (2011) 43e48. M. Govindarajan, M. Rajeswary, Ovicidal and adulticidal potential of leaf and seed extract of Albizia lebbeck (L.) Benth. (Family: Fabaceae) against Culex quinquefasciatus, Aedes aegypti, and Anopheles stephensi (Diptera: Culicidae), Parasitol. Res. 114 (5) (2015) 1949e1961. S. Gurunathan, J.K. Jeong, J. Woong Han, Z.F. Zhang, J.H. Park, J.H. Kim, Multidimensional effects of biologically synthesized silver nanoparticles in Helicobacter pylori, Helicobacter felis, and human lung (L132) and lung carcinoma A549 cells, Nanoscale Res. Let. 10 (2015) 35. M.G. Guzman, M. Mune, G. Kouri, Dengue vaccine: priorities and progress, Expert Rev. Anti Infect. Ther. 2 (2004) 895e911. K.M. Haldar, P. Ghosh, G. Chandra, Larvicidal, adulticidal, repellency and smoke toxic efficacy of Ficus krishnae against Anopheles stephensi Liston and Culex vishnui group mosquito, Asia Pac. J. Trop. Dis. 4 (2014) 214e220. M.C. Hardstone, C.A. Leichter, J.G. Scott, Multiplicative interaction between the two major mechanisms of permethrin resistance, kdr and cytochrome P450-monooxygenase detoxification, in mosquitoes, J. Evol. Biol. 22 (2009) 416e423. K. Kathiresan, B.L. Bingham, Biology of mangroves and mangrove ecosystems, Adv. Mar. Biol. 40 (2001) 81e251. S. Kaviya, J. Santhanalakshmi, B. Viswanathan, J. Muthumary, K. Srinivasan, Biosynthesis of silver nanoparticles using Citrus sinensis peel extract and its antibacterial activity, Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 79 (2011) 594e598. K. Kovendan, K. Murugan, S. Vincent, D.R. Barnard, Studies on larvicidal and pupicidal activity of Leucas aspera Willd (Lamiaceae) and bacterial insecticide, Bacillus sphaericus against malarial vector Anopheles stephensi Liston (Diptera: Culicidae), Parasitol. Res. 110 (2012) 195e203. A.R. Kumar, K.M. Subburathinam, G. Prabakar, Phytochemical screening of selected medicinal plants of Asclepiadaceae family, Asia J. Microbiol. Biotechnol. Environ. Sci. 9 (1) (2007) 177e180. M. Kumar, J. Malik, Pharmacognostical studies and evaluation of quality parameters of Butea frondosa leaves, Inter J. Pharm. Pharm. Sci. 4 (1) (2012) 610e614. S. Li, Y. Shen, A. Xie, X. Yu, L. Qiu, L. Zhang, Q. Zhang, Green synthesis of silver nanoparticles using Capsicum annuum L. extract, Green Chem. 9 (2007) 852e858. P. Madhiyazhagan, K. Murugan, A. Naresh Kumar, T. Nataraj, J. Subramaniam, B. Chandramohan, C. Panneerselvam, D. Dinesh, U. Suresh, M. Nicoletti, M.S. Alsalhi, S. Devanesan, G. Benelli, One pot synthesis of silver nanocrystals using the seaweed Gracilaria edulis: biophysical characterization and potential against the filariasis vector Culex quinquefasciatus and the midge Chironomus circumdatus, J. Appl. Phycol. (2016), http://dx.doi.org/10.1007/ s10811-016-0953-x. M.L. Magwa, G. Mazuru, G. Nyasha, H. Godfred, Chemical composition and biological activities of essential oil from the leaves of Sesuvium portulacastrum, J. Ethnopharmacol. 85 (1) (2000) 103. J.A. Mahyoub, A.T. Aziz, C. Panneerselvam, K. Murugan, M. Roni, S. Trivedi, M. Nicoletti, U.W. Hawas, F.M. Shaher, M.A. Bamakhrama, A. Canale, G. Benelli, Seagrasses as sources of mosquito nanolarvicides? Toxicity and uptake of Halodule uninervis-biofabricated silver nanoparticles in dengue and Zika virus vector Aedes aegypti, J. Clust. Sci. (2016), http://dx.doi.org/ 10.1007/s10876-016-1127-3. H. Mehlhorn (Ed.), Nanoparticles in the Fight against Parasites. Parasitol Res Monographs vol. 8, Springer, Berlin, New York, 2016. A. Mitra, S. Trivedi, S. Zaman, P. Pramanick, S. Chakraborty, N. Pal, P. Fazli, K. Banerjee, Decadal variation of nutrient level in two major estuaries in indian sundarbans, Jord J. Biol. Sci. 8 (3) (2015) 231e236. R.G. Munusamy, D.R. Appadurai, S. Kuppusamy, G.P. Michael, I. Savarimuthu,

[50] [51]

[52]

[53]

[54]

[55]

[56]

[57]

[58]

[59]

[60] [61] [62]

[63]

[64]

[65]

[66]

[67]

[68]

Ovicidal and larvicidal activities of some plant extracts against Aedesaegypti L. and Culex quinquefasciatus Say (Diptera: Culicidae), Asian Pac. J. Trop. Dis. 6 (6) (2016) 468e471. K. Murugan, D. Jeyabalan, Effect of certain plant extracts against the mosquito, Anopheles stephensi Liston, Curr. Sci. 76 (1999) 631e633. K. Murugan, P. Thangamathi, D. Jeyabalan, Interactive effect of botanicals and Bacillus thuringiensis subsp. israelensis on Culex quinquefasciatus Say, J. Sci. Ind. Res. 61 (2003) 1068e1076. K. Murugan, G. Benelli, A. Suganya, D. Dinesh, C. Panneerselvam, M. Nicoletti, J.S. Hwang, P. Mahesh Kumar, J. Subramaniam, U. Suresh, Toxicity of seaweed-synthesized silver nanoparticles against the filariasis vector Culex quinquefasciatus and its impact on predation efficiency of the cyclopoid crustacean Mesocyclops longisetus, Parasitol. Res. 114 (2015a) 2243e2253. K. Murugan, G. Benelli, C. Panneerselvam, J. Subramaniam, T. Jeyalalitha, D. Dinesh, M. Nicoletti, J.S. Hwang, U. Suresh, P. Madhiyazhagan, Cymbopogon citratus-synthesized gold nanoparticles boost the predation efficiency of copepod Mesocyclops aspericornis against malaria and dengue mosquitoes, Exp. Parasitol. 153 (2015b) 129e138. K. Murugan, N. Aarthi, K. Kovendan, C. Panneerselvam, B. Chandramohan, P. Mahesh Kumar, D. Amerasan, M. Paulpandi, R. Chandirasekar, D. Dinesh, U. Suresh, J. Subramaniam, A. Higuchi, A.A. Alarfaj, M. Nicoletti, H. Mehlhorn, G. Benelli, Mosquitocidal and antiplasmodial activity of Senna occidentalis (cassiae) and Ocimum basilicum (Lamiaceae) from maruthamalai hills against Anopheles stephensi and Plasmodium falciparum, Parasitol. Res. 114 (2015c) 3657e3664. K. Murugan, C.M. Samidoss, C. Panneerselvam, A. Higuchi, M. Roni, U. Suresh, B. Chandramohan, J. Subramaniam, P. Madhiyazhagan, D. Dinesh, R. Rajaganesh, A.A. Alarfaj, M. Nicoletti, S. Kumar, H. Wei, A. Canale, H. Mehlhorn, G. Benelli, Seaweed-synthesized silver nanoparticles: an ecofriendly tool in the fight against Plasmodium falciparum and its vector Anopheles stephensi? Parasitol. Res. 114 (2015d) 4087e4097. K. Murugan, D. Dinesh, M. Paulpandi, A.T. Aziz, J. Subramaniam, P. Madhiyazhagan, L. Wang, U. Suresh, P. Mahesh Kumar, J. Mohan, R. Rajaganesh, H. Wei, K. Kalimuthu, M.N. Parajulee, H. Mehlhorn, G. Benelli, Nanoparticles in the fight against mosquito-borne diseases: bioactivity of Bruguiera cylindrica-synthesized nanoparticles against dengue virus DEN-2 in vitro and its mosquito vector Aedes aegypti (Diptera: Culicidae), Parasitol. Res. 114 (2015e) 4349e4361. K. Murugan, P. Aruna, C. Panneerselvam, P. Madhiyazhagan, M. Paulpandi, J. Subramaniam, R. Rajaganesh, H. Wei, M. Saleh Alsalhi, S. Devanesan, M. Nicoletti, B. Syuhei, A. Canale, G. Benelli, Fighting arboviral diseases: low toxicity on mammalian cells, dengue growth inhibition (in vitro) and mosquitocidal activity of Centroceras clavulatum-synthesized silver nanoparticles, Parasitol. Res. 115 (2016a) 651e662. K. Murugan, D. Dinesh, M. Paulpandi, S. Subramaniam J,Rakesh, P. Amuthavalli, C. Panneerselvam, U. Suresh, C. Vadivalagan, M.S. Alsalhi, S. Devanesan, H. Wei, A. Higuchi, M. Nicoletti, A. Canale, G. Benelli, Mangrove helps: Sonneratia alba-synthesized silver nanoparticles magnify guppy fish predation against Aedes aegypti young instars and down-regulate the expression of envelope (E) gene in dengue virus (Serotype DEN-2), J. Clust. Sci. (2016b), http://dx.doi.org/10.1007/s10876-016-1115-7. A. Naresh Kumar, K. Murugan, P. Madhiyazhagan, Integration of botanicals and microbials for management of crop and human pests, Parasitol. Res. 112 (1) (2013) 313e325. €dler, N. Li, Toxic potential of materials at the nano level, A. Nel, T. Xia, L. Ma Science 311 (2006) 622e627. K. Padmakumar, K. Ayyakkannu, Antiviral activity of marine plants, Ind. J. Virol. 13 (1997) 33. Pan American Health Organization, World Health Organization, Neurological Syndrome, Congenital Malformations, and Zika Virus Infection. Implications for Public Health in the Americas-epidemiological Alert, WHO/PAHO, Washington DC, 2015. B.S. Panja, I. Chaudhuri, K. Khanra, N. Bhattacharyya, Biological application of green silver nanoparticle synthesized from leaf extract of Rauvolfia serpentina, Asian Pac. J. Trop. Dis. 6 (7) (2016) 549e556. C. Panneerselvam, K. Murugan, Adulticidal, repellent, and ovicidal properties of indigenous plant extracts against the malarial vector, Anopheles stephensi (Diptera: Culicidae), Parasitol. Res. 112 (2013) 679e692. C. Panneerselvam, K. Murugan, K. Kovendan, P. Mahesh Kumar, S. Ponarulselvam, D. Amerasan, J. Subramaniam, J.S. Hwang, Larvicidal efficacy of Catharanthus roseus Linn. Family: Apocynaceae) leaf extract and bacterial insecticide Bacillus thuringiensis against Anopheles stephensi Liston, Asian Pac. J. Trop. Med. 6 (11) (2013) 847e853. C. Panneerselvam, K. Murugan, M. Roni, A.T. Aziz, U. Suresh, R. Rajaganesh, P. Madhiyazhagan, J. Subramaniam, D. Dinesh, M. Nicoletti, A. Higuchi, A.A. Alarfaj, M.A. Munusamy, S. Kumar, N. Desneux, G. Benelli, Fern-synthesized nanoparticles in the fight against malaria: LC/MS analysis of Pteridium aquilinum leaf extract and biosynthesis of silver nanoparticles with high mosquitocidal and antiplasmodial activity, Parasitol. Res. 115 (2016) 997e1013. S. Patil, S. Mahure, A. Kale, UV, FTIR, HPLC Confirmation of Camptothecin an anticancer metabolite from bark extract of Nothapodytes nimmoniana (J. Graham), Am. J. Ethnomed 1 (3) (2014) 174e185. J.K. Patra, Y.K. Mohanta, Antimicrobial compounds from mangrove plants: a pharmaceutical prospective, Chin. J. Integ. Med. 20 (4) (2014) 311e320.

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002

U. Suresh et al. / Physiological and Molecular Plant Pathology xxx (2017) 1e11 [69] J.K. Patra, H. Thatoi, Anticancer activity and chromatography characterization of methanol extract of Heritiera fomes Buch. Ham a mangrove plant from Bhitarkanika, India, Orient Pharm. Exp. Med. 13 (2013) 133e142. [70] P. Prakash, P. Gnanaprakasam, R. Emmanuel, S. Arokiyaraj, M. Saravanan, Green synthesis of silver nanoparticles from leaf extract of Mimusop selengi, Linn. for enhanced antibacterial activity against multi drug resistant clinical isolates, Colloids Surf. B Biointer. 108 (2013) 255e259. [71] M. Premanthan, K. Chandra, S.K. Bajpai, K. Kathiresan, A survey of some Indian marine plants for antiviral activity, J. Bot. Mar. 321 (1992) 35. [72] H.G. Qin, Z.X. Ye, S.J. Huang, H. Li, Research on the damage by tobacco caterpillar (ProdenialituraFabricius) to cotton and the control threshold, China Cott. 27 (4) (2000) 24e25. [73] M. Ragaei, A.H. Sabry, Nanotechnology for insect pest control, Inter J. Sci. Environ. Technol. 3 (2) (2014) 528e545. [74] J. Raghwani, A. Rambaut, E.C. Holmes, V.T. Hang, T.T. Hien, J. Farrar, B. Wills, N.J. Lennon, B.W. Birren, M.R. Henn, Endemic dengue associated with the cocirculation of multiple viral lineages and localized density-dependent transmission, PLoS Pathog. 7 (2011) e1002064. [75] M. Rai, A. Ingle, Role of nanotechnology in agriculture with special reference to management of insect pests, Appl Microbiol Biotechnol 94 (2012) 287e293. [76] M. Rai, A. Yadav, A. Gade, Silver nanoparticles as a new generation of antimicrobials, BiotechnolAdv 27 (2009) 76e83. [77] R. Rajaganesh, K. Murugan, C. Panneerselvam, S. Jayashanthini, A.T. Aziz, M. Roni, U. Suresh, S. Trivedi, H. Rehman, A. Higuchi, M. Nicoletti, G. Benelli, Fern-synthesized silver nanocrystals: towards a new class of mosquito oviposition deterrents? Res. Vet. Sci. 109 (2016) 40e51. [78] A.J.S. Raju, R. Kumar, On the reproductive ecology of Suaeda maritima, S. monoica, and S. nudiflora (Chenopodiaceae), J. Threat Taxa 8 (6) (2016) 8860e8876. [79] P.U. Rani, K. Sandhyarani, V. Vadlapudi, B. Sreedhar, Bioefficacy of a mangrove plant, Sonneratia caseolaris and a mangrove associate plant, Hibiscus tiliaceus against certain agricultural and stored product pests, J. Biopest. 8 (2) (2015) 98e106. [80] S. Ravikumar, S. Jacob Inbaneson, P. Suganthi, M. Gnanadesigan, In vitro antiplasmodial activity of ethanolic extracts of mangrove plants from South East coast of India against chloroquine-sensitive Plasmodium falciparum, Parasitol. Res. 108 (2011) 873e878. [81] M. Roni, K. Murugan, C. Panneerselvam, J. Subramaniam, M. Nicoletti, P. Madhiyazhagan, D. Dinesh, U. Suresh, H.F. Khater, H. Wei, A. Canale, A.A. Alarfaj, M.A. Munusamy, A. Higuchi, G. Benelli, Characterization and biotoxicity of Hypnea musciformis-synthesized silver nanoparticles as potential eco-friendly control tool against Aedes aegypti and Plutella xylostella, Ecotoxicol. Environ. Saf. 121 (2015) 31e38. [82] A. Sangeetha, U. Saraswathi, G. Singaravelu, Green synthesis of silver nanoparticles using a mangrove Excoecaria agallocha, Inter J. Pharma Sci. Invent 3 (10) (2014) 54e57. [83] K. Satyavani, S. Gurudeeban, T. Ramanathan, T. Balasubramanian, Biomedical potential of silver nanoparticles synthesized from calli cells of Citrullus colocynthis (L.) Schrad, J. Nanobiotechnol. 9 (2011) 43. [84] G. Scrinis, K. Lyons, The emerging nano-corporate paradigm: nanotechnology and the transformation of nature, food and agri-food systems, Int. J. Sociol. Food Agric. 15 (2) (2007) 22e44. [85] K. Shameli, M.B. Ahmad, W.M.Z.W. Yunus, N.A. Ibrahim, Synthesis and characterization of silver/talc nanocomposites using the wet chemical reduction method, Int. J. Nanomed. 5 (2010) 743e751. [86] S. Shanthi, V. Bharathi, G. Hemalatha, E. Rajeshwari, Phytochemical analysis and antibacterial efficacy of Adathoda vasica, World J. Pharm. Pharm. Sci. 5 (3) (2016) 799e808. [87] M. Singh, S. Singh, S. Prasad, I.S. Gambhir, Nanotechnology in medicine and antibacterial effect of silver nanoparticles, Dig. J. NanomaterBiostruct 3 (3) (2008) 115. [89] K.C. Song, S.M. Lee, T.S. Park, B.S. Lee, Preparation of colloidal silver nanoparticles by chemical reduction method, Korean J. Chem. Eng. 26 (1) (2009) 153e155. [90] T. Su, M.S. Mulla, Ovicidal activity of neem products (Azadirachtin) against Culex tarsalis and, Culex quinquefasciatus (Diptera: Culicidae), J. Am. Mosq. Control Assoc. 14 (1998) 204e209. [91] J. Subramaniam, K. Murugan, A. Jebanesan, P. Philips, D. Dinesh, M. Nicoletti, H. Wei, A. Higuchi, S. Kumar, A. Canale, G. Benelli, Do Chenopodium ambrosioides-synthesized silver nanoparticles impact Oryzias melastigma predation against Aedes albopictus Larvae? J. Clust. Sci. (2016) http://dx.doi.org/ 10.1007/s10876-016-1113-9. [92] J. Subramaniam, K. Murugan, C. Panneerselvam, K. Kovendan, P. Madhiyazhagan, D. Dinesh, P. Mahesh Kumar, B. Chandramohan, Multipurpose effectiveness of Couroupita guianensis-synthesized gold nanoparticles: high antiplasmodial potential, field efficacy against malaria vectors

11

and synergy with Aplocheilus lineatus predators, Environ. Sci. Pollut. Res. 23 (8) (2016) 7543e7558, http://dx.doi.org/10.1007/s11356-015-6007-0. [93] U. Suresh, K. Murugan, G. Benelli, M. Nicoletti, D.R. Barnard, C. Panneerselvam, P. Mahesh Kumar, J. Subramaniam, D. Dinesh, B. Chandramohan, Tackling the growing threat of dengue: Phyllanthus nirurimediated synthesis of silver nanoparticles and their mosquitocidal properties against the dengue vector Aedes aegypti (Diptera: Culicidae), Parasitol. Res. 114 (2015) 1551e1562. [94] H. Susanto, Y. Feng, M. Ulbricht, Fouling behavior of aqueous solutions of polyphenolic compounds during ultrafiltration, J. Food Eng. 91 (2009) 333e340. [95] P. Thatoi, R.G. Kerry, S. Gouda, G. Das, K. Pramanik, H. Thatoi, J.K. Patra, Photo-mediated green synthesis of silver and zinc oxide nanoparticles using aqueous extracts of two mangrove plant species, Heritiera fomes and Sonneratia apetala and investigation of their biomedical applications, J. Photochem Photobiol. B Biol. 163 (2016) 311e318. [96] D.K. Tiwari, J. Behari, Biocidal nature of treatment of Ag-nanoparticle and ultrasonic irradiation in Escherichia coli dh5, Adv. Biol. Res. 3 (3e4) (2009) 89e95. [97] S. Trivedi, A.A. Ansari, S.K. Ghosh, H. Rehman, DNA Barcoding in Marine Perspectives, Spring Book, 2016b, http://dx.doi.org/10.1007/978-3-31941840-7. [98] S. Trivedi, S. Zaman, T.R. Chaudhuri, P. Pramanick, P. Fazli, G. Amin, A. Mitra, Inter-annual variation of salinity in indian Sundarbans, Ind. J. Geo-Mar Sci. 45 (3) (2016a) 410e415. [99] H.P. Tsai, Y.Y. Tsai, I.T. Lin, P.H. Kuo, K.C. Chang, J.C. Chen, W.C. Ko, J.R. Wang, Validation and application of a commercial quantitative real-time reverse transcriptase-PCR assay in investigation of a large dengue virus outbreak in southern Taiwan, PLoS Negl. Trop. Dis. 10 (10) (2016) e0005036. [100] J. Umashankari, D. Inbakandan, T.T. Ajithkumar, T. Balasubramanian, Mangrove plant, Rhizophora mucronata (Lamk, 1804) mediated one pot green synthesis of silver nanoparticles and its antibacterial activity against aquatic pathogens, Sal Sys 8 (2012) 11. [101] R. Vahitha, M.R. Venkatachalam, K. Murugan, A. Jebanesan, Larvicidal efficacy of Pavonia zeylanica L. Acacia ferruginea D.C. against Culex quinquefasciatus say, Bioresour. Technol. 82 (2002) 203e204. [102] P. Vinayaga Moorthi, C. Balasubramanian, S. Mohan, An improved insecticidal activity of silver nanoparticle synthesized by using Sargassum muticum, Appl. Biochem. Biotechnol. 175 (2015) 135e140. [103] A. Vineetha, K. Murugan, Larvicidal and smoke repellency effect of Toddalia asiatica and Aegle marmelos against the dengue vector, Aedes aegypti (Insecta: Diptera: Culicidae), Entomol. Res. 39 (2009) 61e65. [104] WHO, Dengue Guidelines for Diagnosis, Treatment, Prevention and Control, World Health Organization, Geneva, 2009. http://www.who.int/iris/handle/ 10665/44188. [105] W. Yang, C. Yang, M. Sun, F. Yang, Y. Ma, Z. Zhang, X. Yang, Green synthesis of nanowire-like Pt nanostructures and their catalytic properties, Talanta 78 (2009) 557e564. [106] Y. Yasur, P. Usha Rani, Lepidopteran insect susceptibility to silver nanoparticles and measurement of changes in their growth, development and physiology, Chemistry 124 (2015) 92e102. [107] N. Yogananth, V. Anuradha, M.Y.S. Ali, R. Muthezhilan, A. Chanthuru, M.M. Prabu, Chemical properties of essential oil from Rhizophora mucronata mangrove leaf against malarial mosquito Anopheles stephensi and filarial mosquito Culex quinquefasciatus, Asian Pac. J. Trop. Dis. 5 (1) (2015) S67eS72. [108] N. Zhang, Y. Yang, H. Lu, X. Ziang, X. Huang, R. Hu, Z. Chen, W. Yuan, R. Peng, J. Peng, H. Ai, K. Liu, Spodoptera litura autophagy-related protein 1 interacts with autophagy-related protein 5 and enhances its degradation, Ins. Mol. Biol. (2016), http://dx.doi.org/10.1111/imb.12284. [109] C.N. Zhou, A progress and development foresight of pesticidal microorganisms in China, Pesticides 40 (2001) 8e10. [110] S.H. Zyoud, Dengue research: a bibliometric analysis of worldwide and Arab publications during 1872e2015, Virol. J. 13 (2016) 78. [111] P. Madhiyazhagan, K. Murugan, A. Naresh Kumar, T. Nataraj, D. Dinesh, C. Panneerselvam, J. Subramaniam, P. Mahesh Kumar, U. Suresh, M. Roni, M. Nicoletti, A.A. Alarfaj, A. Higuchi, M.A. Munusamy, G. Benelli, Sargassum muticum-synthesized silver nanoparticles: an effective control tool against mosquito vectors and bacterial pathogens, Parasitol. Res. (2015), http:// dx.doi.org/10.1007/s00436-015-4671-0. [112] V. Sujitha, K. Murugan, M. Paulpandi, C. Panneerselvam, U. Suresh, M. Roni, M. Nicoletti, A. Higuchi, P. Madhiyazhagan, J. Subramaniam, D. Dinesh, C. Vadivalagan, B. Chandramohan, A.A. Alarfaj, M.A. Munusamy, D.R. Barnard, G. Benelli, Green synthesized silver nanoparticles as a novel control tool against dengue virus (DEN-2) and its primary vector Aedes aegypti, Parasitol. Res. 114 (2015) 3315e3325.

Please cite this article in press as: U. Suresh, et al., Suaeda maritima-based herbal coils and green nanoparticles as potential biopesticides against the dengue vector Aedes aegypti and the tobacco cutworm Spodoptera litura, Physiological and Molecular Plant Pathology (2017), http:// dx.doi.org/10.1016/j.pmpp.2017.01.002