Register      Login
Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH FRONT

Comparing plant–insect trophic transfer of Cu from lab-synthesised nano-Cu(OH)2 with a commercial nano-Cu(OH)2 fungicide formulation

Jieran Li A , Sónia Rodrigues B , Olga V. Tsyusko A C and Jason M. Unrine https://orcid.org/0000-0003-3012-5261 A C D
+ Author Affiliations
- Author Affiliations

A Department of Toxicology and Cancer Biology, University of Kentucky, Lexington, KY 40536, USA.

B Centro de Estudos do Ambiente e do Mar (CESAM) and Department of Chemistry, University of Aveiro, Aveiro 3810-193, Portugal.

C Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA.

D Corresponding author. Email: jason.unrine@uky.edu

Environmental Chemistry 16(6) 411-418 https://doi.org/10.1071/EN19011
Submitted: 15 January 2019  Accepted: 2 March 2019   Published: 29 March 2019

Environmental context. Nanomaterials are being extensively researched for use as agrochemicals, and some commercial formulations containing nanomaterials are already on the market. Information on environmental fate and effects of nanomaterials, however, are largely based on laboratory-synthesised materials. This study questions whether data on trophic transfer of Cu from pure, laboratory-synthesised Cu(OH)2 nanomaterials can be used to predict trophic transfer of Cu from a complex commercial fungicide formulation containing Cu(OH)2 nanomaterials.

Abstract. To examine whether studies conducted with highly purified, laboratory-synthesised nanomaterials are predictive of behaviour of commercial nanopesticide formulations, we studied the trophic transfer of Cu(OH)2 manufactured nanomaterials (MNMs) by tobacco hornworms (Manduca sexta) feeding on surface-treated tomato leaves (Solanum lycopersicum). We compared laboratory-synthesised copper(II) hydroxide (Cu(OH)2) nanowire with the widely used fungicide Kocide® 3000, whose active ingredient is nano-needles of copper(II) hydroxide (nCu(OH)2). All leaves were treated at rates in accordance with the product label (1.5 kg ha−1 or 150 mg m−2). As a control, we used highly soluble CuSO4. Over the course of the study (exposure up to 7 days followed by up to 20 days of elimination), hornworms accumulated Cu from all three treatments far exceeding controls (ranging from ~55 to 105 times greater for nCu(OH)2 and CuSO4 respectively). There were also significant differences in accumulation of Cu among treatments, with the greatest accumulation in the CuSO4 treatment (up to 105 ± 18 μg Cu per g dry mass) and the least in the nCu(OH)2 treatment (up to 55 ± 12 μg Cu per g dry mass. The difference in their toxicity and accumulation and elimination dynamics was found to be correlated with the solubility of the materials in the exposure suspensions (r2 = 0.99). We also found that first-instar larvae are more susceptible to toxicity from all forms of Cu than second-instar larvae. Our results provide valuable knowledge on whether the ecotoxicity of commercial MNM products such as Kocide can be compared with laboratory-synthesised counterparts and suggests that predictions can be made based on functional assays such as measurement of solubility.


References

Adeleye AS, Conway JR, Perez T, Rutten P, Keller AA (2014). Influence of extracellular polymeric substances on the long-term fate, dissolution, and speciation of copper-based nanoparticles. Environmental Science & Technology 48, 12561–12568.
Influence of extracellular polymeric substances on the long-term fate, dissolution, and speciation of copper-based nanoparticlesCrossref | GoogleScholarGoogle Scholar |

Apodaca SA, Tan W, Dominguez OE, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL (2017). Physiological and biochemical effects of nanoparticulate copper, bulk copper, copper chloride, and kinetin in kidney bean (Phaseolus vulgaris) plants. The Science of the Total Environment 599–600, 2085–2094.
Physiological and biochemical effects of nanoparticulate copper, bulk copper, copper chloride, and kinetin in kidney bean (Phaseolus vulgaris) plantsCrossref | GoogleScholarGoogle Scholar | 28558431PubMed |

Aruoja V, Dubourguier H-C, Kasemets K, Annekahru (2009). Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. The Science of the Total Environment 407, 1461–1468.
Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitataCrossref | GoogleScholarGoogle Scholar | 19038417PubMed |

Atha DH, Wang H, Petersen EJ, Cleveland D, Holbrook RD, Jaruga P, Dizdaroglu M, Xing B, Nelson BC (2012). Copper oxide nanoparticle-mediated DNA damage in terrestrial plant models. Environmental Science & Technology 46, 1819–1827.
Copper oxide nanoparticle-mediated DNA damage in terrestrial plant modelsCrossref | GoogleScholarGoogle Scholar |

Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H (2012). Toxicity of silver nanoparticles – nanoparticle or silver ion?. Toxicology Letters 208, 286–292.
Toxicity of silver nanoparticles – nanoparticle or silver ion?Crossref | GoogleScholarGoogle Scholar | 22101214PubMed |

Chen Z, Meng H, Xing G, Chen C, Zhao Y, Jia G, Wang T, Yuan H, Ye C, Zhao F, Chai Z, Zhu C, Fang X, Ma B, Wan L (2006). Acute toxicological effects of copper nanoparticles in vivo. Toxicology Letters 163, 109–120.
Acute toxicological effects of copper nanoparticles in vivoCrossref | GoogleScholarGoogle Scholar | 16289865PubMed |

Congdon JD, Dunham AE, Hopkins WA, Rowe CL, Hinton TG (2001). Resource allocation‐based life histories: a conceptual basis for studies of ecological toxicology. Environmental Toxicology and Chemistry 20, 1698–1703.
Resource allocation‐based life histories: a conceptual basis for studies of ecological toxicologyCrossref | GoogleScholarGoogle Scholar | 11491551PubMed |

Cota-Ruiz K, Hernández-Viezcas JA, Varela-Ramírez A, Valdés C, Núñez-Gastélum JA, Martínez-Martínez A, Delgado-Rios M, Peralta-Videa JR, Gardea-Torresdey JL (2018). Toxicity of copper hydroxide nanoparticles, bulk copper hydroxide, and ionic copper to alfalfa plants: a spectroscopic and gene expression study. Environmental Pollution 243, 703–712.
Toxicity of copper hydroxide nanoparticles, bulk copper hydroxide, and ionic copper to alfalfa plants: a spectroscopic and gene expression studyCrossref | GoogleScholarGoogle Scholar | 30228067PubMed |

Davidowitz G, D’Amico LJ, Nijhout HF (2004). The effects of environmental variation on a mechanism that controls insect body size. Evolutionary Ecology Research 6, 49–62.

Ferry JL, Craig P, Hexel C, Sisco P, Frey R, Pennington PL, Fulton MH, Decho GSAW, Kashiwada S, Murphy CJM, Shaw TJ (2009). Transfer of gold nanoparticles from the water column to the estuarine food web. Nature Nanotechnology 4, 441–444.
Transfer of gold nanoparticles from the water column to the estuarine food webCrossref | GoogleScholarGoogle Scholar | 19581897PubMed |

Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS (2007). Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environmental Science & Technology 41, 8484–8490.
Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubilityCrossref | GoogleScholarGoogle Scholar |

Gardea-Torresdey JL, Rico CM, White JC (2014). Trophic transfer, transformation, and impact of engineered nanomaterials in terrestrial environments. Environmental Science & Technology 48, 2526–2540.
Trophic transfer, transformation, and impact of engineered nanomaterials in terrestrial environmentsCrossref | GoogleScholarGoogle Scholar |

Geisler-Lee J, Wang Q, Yao Y, Zhang W, Geisler M, Li K, Huang Y, Chen Y, Kolmakov A, Ma X (2012). Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicology 7, 323–337.
Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thalianaCrossref | GoogleScholarGoogle Scholar | 22263604PubMed |

Giannousi K, Avramidis I, Dendrinou-Samara C (2013). Synthesis, characterization and evaluation of copper-based nanoparticles as agrochemicals against Phytophthora infestans. RSC Advances 3, 21743–21751.
Synthesis, characterization and evaluation of copper-based nanoparticles as agrochemicals against Phytophthora infestansCrossref | GoogleScholarGoogle Scholar |

Gomes FM, Carvalho DB, Peron AC, Saito K, Miranda K, Machado EA (2012). Inorganic polyphosphates are stored in spherites within the midgut of Anticarsia gemmatalis and play a role in copper detoxification. Journal of Insect Physiology 58, 211–219.
Inorganic polyphosphates are stored in spherites within the midgut of Anticarsia gemmatalis and play a role in copper detoxificationCrossref | GoogleScholarGoogle Scholar | 21946413PubMed |

Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008). Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environmental Toxicology and Chemistry 27, 1972–1978.
Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organismsCrossref | GoogleScholarGoogle Scholar | 18690762PubMed |

Grunert LW, Clarke JW, Ahuja C, Eswaran H, Nijhout HF (2015). A quantitative analysis of growth and size regulation in Manduca sexta: the physiological basis of variation in size and age at metamorphosis. PLoS One 10, e0127988
A quantitative analysis of growth and size regulation in Manduca sexta: the physiological basis of variation in size and age at metamorphosisCrossref | GoogleScholarGoogle Scholar | 26011714PubMed |

Hendren CO, Lowry GV, Unrine JM, Wiesner MR (2015). A functional assay-based strategy for nanomaterial risk forecasting. The Science of the Total Environment 536, 1029–1037.
A functional assay-based strategy for nanomaterial risk forecastingCrossref | GoogleScholarGoogle Scholar | 26188653PubMed |

Hong J, Rico CM, Zhao L, Adeleye AS, Keller AA, Peralta-Videa JR, Gardea-Torresdey JL (2015). Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environmental Science: Processes & Impacts 17, 177–185.
Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa)Crossref | GoogleScholarGoogle Scholar |

Judy JD, Unrine JM, Bertsch PM (2011). Evidence for biomagnification of gold nanoparticles within a terrestrial food chain. Environmental Science & Technology 45, 776–781.
Evidence for biomagnification of gold nanoparticles within a terrestrial food chainCrossref | GoogleScholarGoogle Scholar |

Judy JD, Unrine JM, Rao W, Bertsch PM (2012). Bioaccumulation of gold nanomaterials by Manduca sexta through dietary uptake of surface-contaminated plant tissue. Environmental Science & Technology 46, 12672–12678.
Bioaccumulation of gold nanomaterials by Manduca sexta through dietary uptake of surface-contaminated plant tissueCrossref | GoogleScholarGoogle Scholar |

Kaveh R, Li YS, Ranjbar S, Tehrani R, Brueck CL, Van Aken B (2013). Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ions. Environmental Science & Technology 47, 10637–10644.
Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ionsCrossref | GoogleScholarGoogle Scholar |

Keller AA, Adeleye AS, Conway JR, Garner KL, Zhao L, Cherr GN (2017). Comparative environmental fate and toxicity of copper nanomaterials. NanoImpact 7, 28–40.
Comparative environmental fate and toxicity of copper nanomaterialsCrossref | GoogleScholarGoogle Scholar |

Lee W-M, An Y- J, Yoon H, Kweon H-S (2008). Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environmental Toxicology and Chemistry 27, 1915–1921.
Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticlesCrossref | GoogleScholarGoogle Scholar | 19086317PubMed |

Lewinski NA, Zhu H, Ouyang CR, Conner GP, Wagner DS, Colvin VL, Drezek RA (2011). Trophic transfer of amphiphilic polymer-coated CdSe/ZnS quantum dots to Danio rerio. Nanoscale 3, 3080–3083.
Trophic transfer of amphiphilic polymer-coated CdSe/ZnS quantum dots to Danio rerioCrossref | GoogleScholarGoogle Scholar | 21713272PubMed |

Lu C, Qi L, Yang J, Zhang D, Wu N, Ma J (2004). Simple template-free solution route for the controlled synthesis of Cu(OH)2 and CuO nanostructures. The Journal of Physical Chemistry B 108, 17825–17831.
Simple template-free solution route for the controlled synthesis of Cu(OH)2 and CuO nanostructuresCrossref | GoogleScholarGoogle Scholar |

Luoma SN, Rainbow PS (2005). Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environmental Science & Technology 39, 1921–1931.
Why is metal bioaccumulation so variable? Biodynamics as a unifying conceptCrossref | GoogleScholarGoogle Scholar |

Majumdar S, Trujillo-Reyes J, Hernandez-Viezcas JA, White JC, Peralta-Videa JR, Gardea-Torresdey JL (2016). Cerium biomagnification in a terrestrial food chain: influence of particle size and growth stage. Environmental Science & Technology 50, 6782–6792.
Cerium biomagnification in a terrestrial food chain: influence of particle size and growth stageCrossref | GoogleScholarGoogle Scholar |

Nair PMG, Chung IM (2015). Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.). Ecotoxicology and Environmental Safety 113, 302–313.
Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.)Crossref | GoogleScholarGoogle Scholar |

Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008). Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environmental Science & Technology 42, 8959–8964.
Toxicity of silver nanoparticles to Chlamydomonas reinhardtiiCrossref | GoogleScholarGoogle Scholar |

Nijhout HF, Davidowitz G, Roff DA (2006). A quantitative analysis of the mechanism that controls body size in Manduca sexta. Journal of Biology 5, 16
A quantitative analysis of the mechanism that controls body size in Manduca sextaCrossref | GoogleScholarGoogle Scholar | 16879739PubMed |

Oustriere N, Marchand L, Roulet E, Mench M (2017). Rhizofiltration of a Bordeaux mixture effluent in pilot-scale constructed wetland using Arundo donax L. coupled with potential Cu-ecocatalyst production. Ecological Engineering 105, 296–305.
Rhizofiltration of a Bordeaux mixture effluent in pilot-scale constructed wetland using Arundo donax L. coupled with potential Cu-ecocatalyst productionCrossref | GoogleScholarGoogle Scholar |

Schwabe F, Tanner S, Schulin R, Rotzetter A, Stark W, Von Quadt A, Nowack B (2015). Dissolved cerium contributes to uptake of Ce in the presence of differently sized CeO2 nanoparticles by three crop plants. Metallomics 7, 466–477.
Dissolved cerium contributes to uptake of Ce in the presence of differently sized CeO2 nanoparticles by three crop plantsCrossref | GoogleScholarGoogle Scholar | 25634091PubMed |

Simonin M, Colman BP, Tang W, Judy JD, Anderson SM, Bergemann CM, Rocca JD, Unrine JM, Cassar N, Bernhardt ES (2018). Plant and microbial responses to repeated Cu(OH)2 nanopesticide exposures under different fertilization levels in an agro-ecosystem. Frontiers in Microbiology 9, 1769
Plant and microbial responses to repeated Cu(OH)2 nanopesticide exposures under different fertilization levels in an agro-ecosystemCrossref | GoogleScholarGoogle Scholar | 30108580PubMed |

Skjolding LM, Winther-Nielsen M, Baun A (2014). Trophic transfer of differently functionalized zinc oxide nanoparticles from crustaceans (Daphnia magna) to zebrafish (Danio rerio). Aquatic Toxicology 157, 101–108.
Trophic transfer of differently functionalized zinc oxide nanoparticles from crustaceans (Daphnia magna) to zebrafish (Danio rerio)Crossref | GoogleScholarGoogle Scholar | 25456224PubMed |

Song YF, Huang C, Shi X, Pan YX, Liu X, Luo Z (2016). Endoplasmic reticulum stress and dysregulation of calcium homeostasis mediate Cu-induced alteration in hepatic lipid metabolism of javelin goby Synechogobius hasta. Aquatic Toxicology 175, 20–29.
Endoplasmic reticulum stress and dysregulation of calcium homeostasis mediate Cu-induced alteration in hepatic lipid metabolism of javelin goby Synechogobius hastaCrossref | GoogleScholarGoogle Scholar | 26991751PubMed |

Tan W, Gao Q, Deng C, Wang Y, Lee WY, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL (2018). Foliar exposure of Cu(OH)2 nanopesticide to basil (Ocimum basilicum): variety-dependent copper translocation and biochemical responses. Journal of Agricultural and Food Chemistry 66, 3358–3366.
Foliar exposure of Cu(OH)2 nanopesticide to basil (Ocimum basilicum): variety-dependent copper translocation and biochemical responsesCrossref | GoogleScholarGoogle Scholar | 29558120PubMed |

Tavares KP, Oliveira ÁCD, Vicentini DS, Melegari SP, Matias WG, Barbosa S, Kummrow F (2014). Acute toxicity of copper and chromium oxide nanoparticles to Daphnia similis. Ecotoxicology and Environmental Contamination 9, 43–50.
Acute toxicity of copper and chromium oxide nanoparticles to Daphnia similisCrossref | GoogleScholarGoogle Scholar |

Unrine JM, Shoults-Wilson WA, Zhurbich O, Bertsch PM, Tsyusko OV (2012). Trophic transfer of Au nanoparticles from soil along a simulated terrestrial food chain. Environmental Science & Technology 46, 9753–9760.
Trophic transfer of Au nanoparticles from soil along a simulated terrestrial food chainCrossref | GoogleScholarGoogle Scholar |

Vencalek BE, Laughton SN, Spielman-Sun E, Rodrigues SM, Unrine JM, Lowry GV, Gregory KB (2016). In situ measurement of CuO and Cu(OH)2 nanoparticle dissolution rates in quiescent freshwater mesocosms. Environmental Science & Technology Letters 3, 375–380.
In situ measurement of CuO and Cu(OH)2 nanoparticle dissolution rates in quiescent freshwater mesocosmsCrossref | GoogleScholarGoogle Scholar |

Vijver MG, Gestel CAMV, Lanno RP, Straalen NMV, Peijnenburg WJGM (2004). Internal metal sequestration and its ecotoxicological relevance: a review. Environmental Science & Technology 38, 4705–4712.
Internal metal sequestration and its ecotoxicological relevance: a reviewCrossref | GoogleScholarGoogle Scholar |

Wang Z, Xu L, Zhao J, Wang X, White JC, Xing B (2016). CuO nanoparticle interaction with Arabidopsis thaliana: toxicity, parent–progeny transfer, and gene expression. Environmental Science & Technology 50, 6008–6016.
CuO nanoparticle interaction with Arabidopsis thaliana: toxicity, parent–progeny transfer, and gene expressionCrossref | GoogleScholarGoogle Scholar |

Yokel R, Au T, Macphail R, Hardas SS, Butterfield DA, Sultana R, Goodman M, Tseng M, Dan M, Haghnazar H, Unrine J, Graham U, Wu P, Grulke E (2012). Distribution, elimination and biopersistence to 90 days of a systemically introduced 30-nm ceria engineered nanomaterial in rats. Toxicological Sciences 127, 256–268.
Distribution, elimination and biopersistence to 90 days of a systemically introduced 30-nm ceria engineered nanomaterial in ratsCrossref | GoogleScholarGoogle Scholar | 22367688PubMed |

Zhao L, Huang Y, Hannah-Bick C, Fulton AN, Keller AA (2016). Application of metabolomics to assess the impact of Cu(OH)2 nanopesticide on the nutritional value of lettuce (Lactuca sativa): enhanced Cu intake and reduced antioxidants. NanoImpact 3–4, 58–66.
Application of metabolomics to assess the impact of Cu(OH)2 nanopesticide on the nutritional value of lettuce (Lactuca sativa): enhanced Cu intake and reduced antioxidantsCrossref | GoogleScholarGoogle Scholar |

Zhao L, Hu Q, Huang Y, Fulton AN, Hannah-Bick C, Adeleye AS, Keller AA (2017a). Activation of antioxidant and detoxification gene expression in cucumber plants exposed to a Cu(OH)2 nanopesticide. Environmental Science: Nano 4, 1750–1760.
Activation of antioxidant and detoxification gene expression in cucumber plants exposed to a Cu(OH)2 nanopesticideCrossref | GoogleScholarGoogle Scholar |

Zhao X, Yu M, Xu D, Liu A, Hou X, Hao F, Long Y, Zhou Q, Jiang G (2017b). Distribution, bioaccumulation, trophic transfer, and influences of CeO2 nanoparticles in a constructed aquatic food web. Environmental Science & Technology 51, 5205–5214.
Distribution, bioaccumulation, trophic transfer, and influences of CeO2 nanoparticles in a constructed aquatic food webCrossref | GoogleScholarGoogle Scholar |

Zhao L, Huang Y, Keller AA (2018). Comparative metabolic response between cucumber (Cucumis sativus) and corn (Zea mays) to a Cu(OH)2 nanopesticide. Journal of Agricultural and Food Chemistry 66, 6628–6636.
Comparative metabolic response between cucumber (Cucumis sativus) and corn (Zea mays) to a Cu(OH)2 nanopesticideCrossref | GoogleScholarGoogle Scholar | 28493687PubMed |

Zuverza-Mena N, Medina-Velo IA, Barrios AC, Tan W, Peralta-Videa JR, Gardea-Torresdey JL (2015). Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum). Environmental Science: Processes & Impacts 17, 1783–1793.
Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum)Crossref | GoogleScholarGoogle Scholar |