Iron and iron oxide nanoparticles are highly toxic to Culex quinquefasciatus with little non-target effects on larvivorous fishes

The control of filariasis vectors has been enhanced in several areas, but there are main challenges, including increasing resistance to insecticides and lack of cheap and eco-friendly products. The toxicity of iron (Fe0) and iron oxide (Fe2O3) nanoparticles has been scarcely investigated yet. We studied the larvicidal and pupicidal activity of Fe0 and Fe2O3 nanoparticles against Culex quinquefasciatus. Fe0 and Fe2O3 nanoparticles produced by green (using a Ficus natalensis aqueous extract) and chemical nanosynthesis, respectively, were analyzed by UV–Vis spectrophotometry, FT-IR spectroscopy, XRD analysis, SEM, and EDX assays. In larvicidal and pupicidal experiments on Cx. quinquefasciatus, LC50 of Fe0 nanoparticles ranged from 20.9 (I instar larvae) to 43.7 ppm (pupae) and from 4.5 (I) to 22.1 ppm (pupae) for Fe2O3 nanoparticles synthesized chemically. Furthermore, the predation efficiency of the guppy fish, Poecilia reticulata, after a single treatment with sub-lethal doses of Fe0 and Fe2O3 nanoparticles was magnified. Overall, this work provides new insights about the toxicity of Fe0 and Fe2O3 nanoparticles against mosquito vectors; we suggested that green and chemical fabricated nano-iron may be considered to develop novel and effective pesticides.

[1]  G. Benelli,et al.  Special Issue: Applications of Green-Synthesized Nanoparticles in Pharmacology, Parasitology and Entomology , 2017, Journal of Cluster Science.

[2]  S. Mandal,et al.  Studies on antibacterial activity of Ficus racemosa Linn. leaf extract , 2000, Phytotherapy research : PTR.

[3]  G. Benelli,et al.  Acute larvicidal toxicity of five essential oils (Pinus nigra, Hyssopus officinalis, Satureja montana, Aloysia citrodora and Pelargonium graveolens) against the filariasis vector Culex quinquefasciatus: Synergistic and antagonistic effects. , 2017, Parasitology international.

[4]  Sudhakar R. Sainkar,et al.  Fungus-mediated synthesis of silver nanoparticles and their immobilization in the mycelial matrix: a novel biological approach to nanoparticle synthesis , 2001 .

[5]  S. Tennyson,et al.  Laboratory Evaluation of Two Meliaceae Species as Larvicides Against Culex quinquefasciatus Say (Diptera: Culicidae) , 2016 .

[6]  R. A. Laskar,et al.  Biogenic synthesis of Au and Ag nanoparticles using aqueous solutions of Black Tea leaf extracts. , 2009, Colloids and surfaces. B, Biointerfaces.

[7]  G. Benelli,et al.  Curzerene, trans-β-elemenone, and γ-elemene as effective larvicides against Anopheles subpictus, Aedes albopictus, and Culex tritaeniorhynchus: toxicity on non-target aquatic predators , 2018, Environmental Science and Pollution Research.

[8]  Jaya Lakkakula,et al.  Extracellular synthesis of silver nanoparticles using dried leaves of pongamia pinnata (L) pierre , 2010 .

[9]  M. Joya,et al.  Preparation and characterization of Fe2O3 nanoparticles , 2013 .

[10]  Jiang‐Shiou Hwang,et al.  Biosynthesis, characterization, and acute toxicity of Berberis tinctoria-fabricated silver nanoparticles against the Asian tiger mosquito, Aedes albopictus, and the mosquito predators Toxorhynchites splendens and Mesocyclops thermocyclopoides , 2015, Parasitology Research.

[11]  G. Benelli,et al.  Toxicity of ar-curcumene and epi-β-bisabolol from Hedychium larsenii (Zingiberaceae) essential oil on malaria, chikungunya and St. Louis encephalitis mosquito vectors. , 2017, Ecotoxicology and environmental safety.

[12]  K. Shameli,et al.  Green Synthesis of Magnetite (Fe3O4) Nanoparticles Using Seaweed (Kappaphycus alvarezii) Extract , 2016, Nanoscale Research Letters.

[13]  R. Pavela.  Essential oils for the development of eco-friendly mosquito larvicides: A review , 2015 .

[14]  Saswati Saha,et al.  PRODUCTION OF SILVER NANOPARTICLES BY A PHYTOPATHOGENIC FUNGUS BIPOLARIS NODULOSA AND ITS ANTIMICROBIAL ACTIVITY , 2010 .

[15]  D. A. Russell,et al.  Energy-dispersive X-ray analysis of the extracellular cadmium sulfide crystallites of Klebsiella aerogenes , 1995, Archives of Microbiology.

[16]  A. Ghosh,et al.  Mosquito larvicidal and antimicrobial activity of synthesized nano-crystalline silver particles using leaves and green berry extract of Solanum nigrum L. (Solanaceae: Solanales). , 2013, Acta tropica.

[17]  G. Benelli,et al.  Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control , 2016, Parasitology Research.

[18]  H. Lai,et al.  Preparation of Monodisperse Iron Oxide Nanoparticles via the Synthesis and Decomposition of Iron Fatty Acid Complexes , 2009, Nanoscale research letters.

[19]  A. A. Rahuman,et al.  Efficacy of larvicidal botanical extracts against Culex quinquefasciatus Say (Diptera: Culicidae) , 2009, Parasitology Research.

[20]  H. Vali,et al.  Extracellular synthesis of magnetite and metal-substituted magnetite nanoparticles. , 2006, Journal of nanoscience and nanotechnology.

[21]  M. Sharon,et al.  Nanotechnology in agricultural diseases and food safety. , 2010 .

[22]  M. Hedimbi,et al.  An ethnobotanical survey of plants used to manage HIV/AIDS opportunistic infections in Katima Mulilo, Caprivi region, Namibia , 2010, Journal of ethnobiology and ethnomedicine.

[23]  J. Dalziel,et al.  The useful plants of West Tropical Africa. , 1938 .

[24]  Muhammad Akhyar Farrukh,et al.  Photodegradation of 2,4,6-trinitrophenol catalyzed by Zn/MgO nanoparticles prepared in aqueous-organic medium , 2013, Korean Journal of Chemical Engineering.

[25]  G. Benelli,et al.  Larvicidal activity of Blumea eriantha essential oil and its components against six mosquito species, including Zika virus vectors: the promising potential of (4E,6Z)-allo-ocimene, carvotanacetone and dodecyl acetate , 2017, Parasitology Research.

[26]  L. Love,et al.  Magnetic properties of biosynthesized magnetite nanoparticles , 2005, IEEE Transactions on Magnetics.

[27]  G. Benelli,et al.  Toxicity on Dengue Mosquito Vectors Through Myristica fragrans-Synthesized Zinc Oxide Nanorods, and Their Cytotoxic Effects on Liver Cancer Cells (HepG2) , 2016, Journal of Cluster Science.

[28]  Se-Won Park,et al.  Immunotoxicity activity of natural furocoumarins from milky sap of Ficus carica L. against Aedes aegypti L. , 2011, Immunopharmacology and immunotoxicology.

[29]  R. Ramanibai,et al.  Bioactive compound synthesis of Ag nanoparticles from leaves of Melia azedarach and its control for mosquito larvae. , 2015, Research in veterinary science.

[30]  D. Oliver,et al.  South African traditional herbal medicines used during pregnancy and childbirth. , 1992, Journal of ethnopharmacology.

[31]  A. A. Rahuman,et al.  Larvicidal activity of green synthesized silver nanoparticles using bark aqueous extract of Ficus racemosa against Culex quinquefasciatus and Culex gelidus. , 2013, Asian Pacific journal of tropical medicine.

[32]  Dina M Fonseca,et al.  "Bird biting" mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. , 2011, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[33]  V. Titanji,et al.  The antimalarial potential of medicinal plants used for the treatment of malaria in Cameroonian folk medicine. , 2008, African journal of traditional, complementary, and alternative medicines : AJTCAM.

[34]  J. van Staden,et al.  Antibacterial activity of South African plants used for medicinal purposes. , 1997, Journal of ethnopharmacology.

[35]  J. Tabuti.  The uses, local perceptions and ecological status of 16 woody species of Gadumire Sub-county, Uganda , 2007, Biodiversity and Conservation.

[36]  P. Velur,et al.  BIOGENIC SYNTHESIS OF Fe3O4 NANOPARTICLES USING TRIDAX PROCUMBENS LEAF EXTRACT AND ITS ANTIBACTERIAL ACTIVITY ON PSEUDOMONAS AERUGINOSA , 2012 .

[37]  A. Anyamba,et al.  Rift Valley Fever: An Emerging Mosquito-Borne Disease. , 2016, Annual review of entomology.

[38]  B. Viswanathan,et al.  Thermal decomposition as route for silver nanoparticles , 2006, Nanoscale research letters.

[39]  M. Alsalhi,et al.  Multipurpose effectiveness of Couroupita guianensis-synthesized gold nanoparticles: high antiplasmodial potential, field efficacy against malaria vectors and synergy with Aplocheilus lineatus predators , 2016, Environmental Science and Pollution Research.

[40]  A. Higuchi,et al.  Rapid biosynthesis of silver nanoparticles using Crotalaria verrucosa leaves against the dengue vector Aedes aegypti: what happens around? An analysis of dragonfly predatory behaviour after exposure at ultra-low doses , 2016, Natural product research.

[41]  J. Sjöblom,et al.  Sol/Gel Glass with Ferric Nitrate Hydrate Temperature Dependence Transition II) high concentration of iron in the glass , 1998 .

[42]  A. Higuchi,et al.  Characterization and biotoxicity of Hypnea musciformis-synthesized silver nanoparticles as potential eco-friendly control tool against Aedes aegypti and Plutella xylostella. , 2015, Ecotoxicology and environmental safety.

[43]  G. Benelli,et al.  Exploring genetic variation in haplotypes of the filariasis vector Culex quinquefasciatus (Diptera: Culicidae) through DNA barcoding. , 2017, Acta tropica.

[44]  G. Benelli.  Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer-a brief review. , 2016, Enzyme and microbial technology.

[45]  D. Goia,et al.  Silver nanoparticles for printable electronics and biological applications , 2009 .

[46]  G. Benelli,et al.  Commentary: Making Green Pesticides Greener? The Potential of Plant Products for Nanosynthesis and Pest Control , 2016, Journal of Cluster Science.

[47]  C. Robic,et al.  Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. , 2008, Chemical reviews.

[48]  M. Noruzi,et al.  A rapid biosynthesis route for the preparation of gold nanoparticles by aqueous extract of cypress leaves at room temperature. , 2012, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[49]  G. Benelli.  Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review , 2015, Parasitology Research.

[50]  Jiang‐Shiou Hwang,et al.  Biosynthesis, mosquitocidal and antibacterial properties of Toddalia asiatica-synthesized silver nanoparticles: do they impact predation of guppy Poecilia reticulata against the filariasis mosquito Culex quinquefasciatus? , 2015, Environmental Science and Pollution Research.

[51]  R. Wrangham,et al.  Zoopharmacognosy: the use of medicinal plants by animals , 1993 .

[52]  A. Saxena,et al.  BIOLOGICAL SYNTHESIS OF SILVER NANOPARTICLES BY USING ONION (ALLIUM CEPA) EXTRACT AND THEIR ANTIBACTERIAL ACTIVITY , 2010 .

[53]  T. Pradeep,et al.  Coalescence of Nanoclusters and Formation of Submicron Crystallites Assisted by Lactobacillus Strains , 2002 .

[54]  G. Benelli,et al.  Current vector control challenges in the fight against malaria. , 2017, Acta tropica.

[55]  Balachandran Unni Nair,et al.  Microwave assisted template synthesis of silver nanoparticles , 2008 .

[56]  J. Gaddum.  Probit Analysis , 1948, Nature.

[57]  R. Messing,et al.  Predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector, Aedes aegypti, in an aquatic environment treated with mosquitocidal nanoparticles , 2015, Parasitology Research.

[58]  Muhammad Nadir Naqqash,et al.  Insecticide resistance and its molecular basis in urban insect pests , 2016, Parasitology Research.

[59]  X. Jing,et al.  Formation mechanism and optimization of highly luminescent N-doped graphene quantum dots , 2014, Scientific Reports.

[60]  P. Chung,et al.  Combined effect of biopesticides on the digestive enzymatic profiles of Cnaphalocrocis medinalis (Guenée) (the rice leaffolder) (Insecta: Lepidoptera: Pyralidae). , 2006, Ecotoxicology and environmental safety.

[61]  C. Patil,et al.  Larvicidal activity of silver nanoparticles synthesized using Plumeria rubra plant latex against Aedes aegypti and Anopheles stephensi , 2011, Parasitology Research.

[62]  Yunyi Fu,et al.  Synthesis of Fe2O3 nanowires by oxidation of iron , 2001 .

[63]  Giovanni Benelli,et al.  Research in mosquito control: current challenges for a brighter future , 2015, Parasitology Research.

[64]  Y. R. Lee,et al.  Sonochemically synthesized ferromagnetic Fe3O4 nanoparticles as a recyclable catalyst for the preparation of pyrrolo[3,4-c]quinoline-1,3-dione derivatives , 2014 .

[65]  E. J. Al-Kalifawi,et al.  Green synthesis of Magnetite Iron Oxide Nanoparticles by Using Al-Abbas's (A.S.) Hund Fruit (Citrus medica) var. Sarcodactylis Swingle Extract and Used in Al-'alqami River Water Treatment , 2015 .

[66]  G. Benelli,et al.  Artemisia absinthium-borne compounds as novel larvicides: effectiveness against six mosquito vectors and acute toxicity on non-target aquatic organisms , 2016, Parasitology Research.

[67]  A. Higuchi,et al.  Green-synthesized silver nanoparticles as a novel control tool against dengue virus (DEN-2) and its primary vector Aedes aegypti , 2015, Parasitology Research.

[68]  M. Starowicz,et al.  Electrochemical synthesis of silver nanoparticles , 2006 .

[69]  K. Tharani,et al.  Synthesis and Characterization of Iron Oxide Nanoparticle by Precipitation Method , 2015 .

[70]  Absar Ahmad,et al.  Rapid synthesis of Au, Ag, and bimetallic Au core-Ag shell nanoparticles using Neem (Azadirachta indica) leaf broth. , 2004, Journal of colloid and interface science.

[71]  M. Faizal,et al.  Synthesis and Properties of Fe3O4 Nanoparticles by Co-precipitation Method to Removal Procion Dye , 2013 .

[72]  C. Stefanini,et al.  Nanoparticles as effective acaricides against ticks-A review. , 2017, Ticks and tick-borne diseases.

[73]  P. Singariya,et al.  Antimicrobial Activity of the Crude Extracts of Withania somnifera and Cenchrus setigerus In-vitro , 2012 .

[74]  Balaprasad Ankamwar,et al.  Biological synthesis of triangular gold nanoprisms , 2004, Nature materials.

[75]  L. Angenot,et al.  Evaluation of 13 selected medicinal plants from Burkina Faso for their antiplasmodial properties. , 2010, Journal of ethnopharmacology.

[76]  C. Patil,et al.  Larvicidal activity of silver nanoparticles synthesized using Pergularia daemia plant latex against Aedes aegypti and Anopheles stephensi and nontarget fish Poecillia reticulata , 2012, Parasitology Research.

[77]  G. Benelli,et al.  Exploitation of chemical, herbal and nanoformulated acaricides to control the cattle tick, Rhipicephalus (Boophilus) microplus - A review. , 2017, Veterinary parasitology.

[78]  Anjum Fatma,et al.  Rapid synthesis of silver nanoparticles using dried medicinal plant of basil. , 2010, Colloids and surfaces. B, Biointerfaces.

[79]  Y. R. Lee,et al.  Green fabrication of ferromagnetic Fe3O4 nanoparticles and their novel catalytic applications for the synthesis of biologically interesting benzoxazinone and benzthioxazinone derivatives , 2014 .

[80]  A. A. Rahuman,et al.  Larvicidal activity of synthesized silver nanoparticles using Eclipta prostrata leaf extract against filariasis and malaria vectors. , 2011, Acta tropica.

[81]  N. Lall,et al.  Antimicrobial activity of the crude extracts and compounds from Ficus chlamydocarpa and Ficus cordata (Moraceae). , 2008, Journal of ethnopharmacology.

[82]  H. Gelderblom.  Lymphatic filariasis: the disease and its control. Fifth report of the WHO Expert Committee on Filariasis. , 1992, World Health Organization technical report series.

[83]  H. Mehlhorn,et al.  Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae) , 2006, Parasitology Research.

[84]  Q. Pankhurst,et al.  Applications of magnetic nanoparticles in biomedicine , 2003 .

[85]  V. Kuete,et al.  Antimicrobial activity of the crude extract, fractions and compounds from stem bark of Ficus ovata (Moraceae). , 2009, Journal of ethnopharmacology.

[86]  Jiang‐Shiou Hwang,et al.  Cymbopogon citratus-synthesized gold nanoparticles boost the predation efficiency of copepod Mesocyclops aspericornis against malaria and dengue mosquitoes. , 2015, Experimental parasitology.

[87]  Jiang‐Shiou Hwang,et al.  Toxicity of seaweed-synthesized silver nanoparticles against the filariasis vector Culex quinquefasciatus and its impact on predation efficiency of the cyclopoid crustacean Mesocyclops longisetus , 2015, Parasitology Research.

[88]  R. Yuvakkumar,et al.  Green Synthesis of Spinel Magnetite Iron Oxide Nanoparticles , 2014 .

[89]  Ning Gu,et al.  Biosynthesis of gold nanoparticles using the bacteria Rhodopseudomonas capsulata , 2007 .

[90]  M. Pileni,et al.  Synthesis of Highly Monodisperse Silver Nanoparticles from AOT Reverse Micelles: A Way to 2D and 3D Self-Organization , 1997 .

[91]  G. Chandra,et al.  Fabrication, characterization and mosquito larvicidal bioassay of silver nanoparticles synthesized from aqueous fruit extract of putranjiva, Drypetes roxburghii (Wall.) , 2013, Parasitology Research.

[92]  Yang Ren,et al.  Preparation and application of magnetic Fe3O4 nanoparticles for wastewater purification , 2009 .

[93]  R. Pavela.  Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae , 2015, Parasitology Research.

[94]  G. Benelli,et al.  One-pot fabrication of silver nanocrystals using Nicandra physalodes: A novel route for mosquito vector control with moderate toxicity on non-target water bugs. , 2016, Research in veterinary science.

[95]  A. Higuchi,et al.  Magnetic nanoparticles are highly toxic to chloroquine-resistant Plasmodium falciparum, dengue virus (DEN-2), and their mosquito vectors , 2017, Parasitology Research.

[96]  Jiang‐Shiou Hwang,et al.  Mosquito control with green nanopesticides: towards the One Health approach? A review of non-target effects , 2018, Environmental Science and Pollution Research.

[97]  G. Malucelli.  Polymer Analysis , 2019, Polymers.

[98]  H. Mehlhorn,et al.  Repellency effect of forty-one essential oils against Aedes, Anopheles, and Culex mosquitoes , 2006, Parasitology Research.

[99]  G. Benelli.  Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review , 2015, Parasitology Research.

[100]  G. Benelli,et al.  Mosquito vectors of Zika virus , 2017 .

[101]  V. Mody,et al.  Introduction to metallic nanoparticles , 2010, Journal of pharmacy & bioallied sciences.

[102]  G. Benelli,et al.  Single-step biosynthesis and characterization of silver nanoparticles using Zornia diphylla leaves: A potent eco-friendly tool against malaria and arbovirus vectors. , 2016, Journal of photochemistry and photobiology. B, Biology.

[103]  M. Arasu,et al.  Enhanced antibacterial activity of iron oxide magnetic nanoparticles treated with Argemone mexicana L. leaf extract: An in vitro study , 2013 .

[104]  M. Iwu,et al.  Handbook of African Medicinal Plants , 2014 .

[105]  Giovanni Benelli,et al.  Commentary: Data Analysis in Bionanoscience—Issues to Watch for , 2016, Journal of Cluster Science.

[106]  Siavash Iravani,et al.  Green synthesis of metal nanoparticles using plants , 2011 .

[107]  G. Benelli,et al.  Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints. , 2016, Trends in plant science.

[108]  G. Benelli,et al.  Mosquitocidal and antibacterial activity of green-synthesized silver nanoparticles from Aloe vera extracts: towards an effective tool against the malaria vector Anopheles stephensi? , 2015, Parasitology Research.