Effect of heavy metals (Cd, Cu, and Zn) on feeding indices and energy reserves of the cotton boll worm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae)

Open access


Third-instar larvae of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) were exposed to 12.5, 25, and 50 mg/kg concentrations of cadmium (Cd). The third-instar larvae were also exposed to 25, 50, and 100 mg/kg concentration of copper (Cu), and 25, 50, and 100 mg/kg concentrations of zinc (Zn). The heavy metal concentrations were each introduced separately into the artificial diet of the third-instar larvae. The third-instar larvae were 24 h old at the start of the treatment. The larvae were maintained in controlled conditions (26±1°C, 65±10% RH and 16L : 8D h) for 7 days. The feeding indices and the level of total protein, glycogen, cholesterol, and triglyceride were measured after the treatments. The results showed that high concentrations of Cd significantly increased approximate digestibility (AD). The relative growth rate (RGR) was significantly enhanced with a 25 mg/kg concentration of Cu. Efficiency of conversion of the ingested food (ECI%) increased significantly with lower concentrations of copper (25 and 50 mg/kg). The amount of cholesterol was also enhanced with 12.5 and 25 mg/kg concentrations of cadmium while the amount of triglyceride was significantly reduced in all Cd treatments. Glycogen, protein, and cholesterol were significantly enhanced in all Cu treatments. The amount of triglycerides at 25 and 50 mg/kg of Cu was significantly increased. Glycogen in all Zn treatments was significantly increased. Protein and cholesterol levels showed significant reduction with a 25 and 50 mg/kg concentration of zinc while triglyceride was enhanced with a 50 mg/kg concentration of Zn. It is clear from the present results that the presence of such heavy metals in the environment has an intense impact on H. armigera as far as food consumption and biochemical indices are concerned. Therefore, a need is shown for a more comprehensive study on the life table and immunology of this insect, under the presence of heavy metals.

Bagatto G., Shorthouse J.D. 1996. Accumulation of Cu and Ni in successive stages of Lymantria dispar L. (Lymantriidae: Lepidoptera) near ore smelters at Sudbury, Ontario, Canada. Environ. Pollut. 92 (1): 7–12.

Bischof C. 1995. Effects of heavy metal stress on carbohydrate and lipid concentrations in the haemolymph and total body tissue of parasitized Lymantria dispar L. larvae (Lepidoptera). Com. Biochem. Physiol. 112 (1): 87–92.

Boyd R.S. 2010. Heavy metal pollutants and chemical ecology: exploring new frontiers. J. Chem. Ecol. 36 (1): 46–58.

Cass A., Hill H. 1980. Copper proteins and copper enzymes. p. 71–85. In: “Biological Roles of Copper”. CIBA Foundation Symposium 79, London, UK, 352 pp.

Cervera A., Maymo A., Sendra M., Martinez-Pardo R., Garcera M. 2004. Cadmium effects on development and reproduction of Oncopeltus fasciatus (Heteroptera: Lygaeidae). J. Insect Physiol. 50 (8): 737–749.

Chang H.Y., Sun B.Y., Liu C.S. 2000. Advances in the study of plants copper toxicity. J. Shandong Agric. Univ. 31: 227–230.

Chen P. 1985. Amino acid and protein metabolism. p. 177–199.

In: “Comprehensive Insect Physiology, Biochemistry, and Pharmacology” (G.A. Kerkut, L.I. Gilbert, eds.). Pergamon Press, Oxford, UK, 8536 pp.

Cheruiyot D.J., Boyd R.S., Coudron T.A., Cobine P.A. 2013. Bioaccumulation and effects of herbivore dietary Co, Cu, Ni, and Zn on growth and development of the insect predator Podisus maculiventris (Say). J. Chem. Ecol. 39 (6): 764–772.

Dadd R.H. 1985. Nutrition: organisms. p. 313–390. In: “Comprehensive Insect Physiology, Biochemistry and Pharmacology” (G.A. Kerkut, L.I. Gilbert, eds.). Pergamon Press. Oxford, UK, 8536 pp.

De Moor J., Koropatnick D. 2000. Metals and cellular signaling in mammalian cells. Cel. Mol. Biol. (Noisy-le-Grand, France) 46 (2): 367–381.

Deng H., Ye Z., Wong M. 2004. Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environ. Pollut. 132 (1): 29–40.

Depledge M., Rainbow P. 1990. Models of regulation and accumulation of trace metals in marine invertebrates. Comp. Biochem. Physiol. 97 (1): 1–7.

Emre I., Kayis T., Coskun M., Dursun O., Cogun H.Y. 2013. Changes in antioxidative enzyme activity, glycogen, lipid, protein, and malondialdehyde content in cadmium-treated Galleria mellonella larvae. Ann. Entomol. Soc. Am. 106 (3): 371–377.

Fountain M.T., Hopkin S.P. 2001. Continuous monitoring of Folsomia candida (Insecta: Collembola) in a metal exposure test. Ecotoxicol. Eviron. Saf. 48 (3): 275–286.

Funk A.E., Day F.A., Brady F.O. 1987. Displacement of zinc and copper from copper-induced metallothionein by cadmium and by mercury: In vivo and ex vivo studies. Comp. Biochem. Physiol. 86 (1): 1–6.

Hackman R. 1974. Chemistry of the insect cuticle. p. 215–270. In: “The Physiology of Insecta”. 2nd ed. (M. Rockstein, ed.). Academic Press, Inc., London, UK, 535 pp.

Hare L. 1992. Aquatic insects and trace metals: bioavailability, bioaccumulation and toxicity. CRC Cr. Rev. Toxcicol. 22 (5–6): 327–369.

Hemati S., Naseri B., Ganbalani G.N., Dastjerdi H.R., Golizadeh A. 2012. Effect of different host plants on nutritional indices of the pod borer, Helicoverpa armigera. J. Insect Sci. 12 (55): 1–15.

Hogervorst P.A., Wäckers F.L., Romeis J. 2007. Effects of honeydew sugar composition on the longevity of Aphidius ervi. Entomol. Exp. Appl. 122 (3): 223–232.

Huang D., Kong J., Seng Y. 2012. Effects of the heavy metal Cu2+ on growth, development, and population dynamics of Spodoptera litura (Lepidoptera: Noctuidae). J. Econ. Entomol. 105 (1): 288–294.

Ilijin L., Periać-Mataruga V., Radojičić R., Lazarević J., Nenadović V., Vlahović M., Mrdaković M. 2009. Effects of cadmium on protocerebral neurosecretory neurons and fitness components in Lymantria dispar L. Folia. Biol. (Krakow) 58 (1–2): 91–99.

Jensen P., Trumble J.T. 2003. Ecological consequences of bioavailability of metals and metalloids in insects. Recent Res. Dev. Entomol. 42: 1–17.

Kagi J., Kojima Y. 1986. Chemistry and biochemistry of metallothionein. Experientia Suppl. 52: 25–61.

King A.B.S. 1994. Heliothis/Helicoverpa (Lepidoptera: Noctuidae). p. 39–106. In: “Insect Pests of Cotton” (G.A. Matthews, J.P. Tunstall, eds.). CAB Int., Wallingford, UK, 593 pp.

Lagadic L., Caquet T., Ramade F. 1994. The role of biomarkers in environmental assessment. Invertebrate populations and communities. Ecotoxicology 3 (3): 193–208.

Lindqvist L. 1992. Accumulation of cadmium, copper, and zinc in five species of phytophagous insects. Environ. Entomol. 21 (1): 160–163.

Liu J., Dong Y., Xu H ,.Wang D., Xu J. 2007. Accumulation of Cd, Pb and Zn by 19 wetland plant species in constructed wetland. J. Hazard. Mater. 147 (3): 947–953.

Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1): 265–275.

Lu G., Di S., Xueping Z. 2011. Analysis on the current pollution situation of Cu, Pb and Zn in the cultivated black soil of songnen plain. Chin. Agric. Sci. Bull. 27 (6): 261–265.

Marino F., Stürzenbaum S., Kille P., Morgan A. 1998. Cu–Cd interactions in earthworms maintained in laboratory microcosms: the examination of a putative copper paradox. Comp. Biochem. Physiol. 120 (2): 217–223.

Maroni G., Lastowski-Perry D., Otto E., Watson D. 1986. Effects of heavy metals on Drosophila larvae and a metallothionein cDNA. Environ. Health Perspect. 65: 107–116.

Marshall A. 1983. X-ray microanalysis of copper and sulphurcontaining granules in the fat body cells of homopteran insects. Tissue Cell 15 (2): 311–315.

Maryanski M., Kramarz P., Laskowski R., Niklinska M. 2002. Decreased energetic reserves, morphological changes and accumulation of metals in carabid beetles (Poecilus cupreus L.) exposed to zinc-or cadmium-contaminated food. Ecotoxicology 11 (2): 127–139.

Matthews N. 1999. Heliothine Moths of Australia. CSIRO Publishing, Canaberra, Australia, 320 pp.

McFarlane J. 1974. The functions of copper in the house cricket and the relation of copper to vitamin E. Can. Entomol. 106 (4): 441–446.

Mitterbock F., Fuhrer E. 1988. Effects of fluoride-polluted spruce leaves on nun moth caterpillars (Lymantria monacha). J. Appl. Entomol. 105 (1): 19–27.

Nation J.L. 2008. Insect Physiology and Biochemistry. 2nd ed. CRC Press, New York, USA, 544 pp.

Nazir A., Malik R.N., Ajaib M., Khan N., Siddiqui M.F. 2011. Hyperaccumulators of heavy metals of industrial areas of Islamabad and Rawalpindi. Pakistan J. Bot. 43 (4): 1925–1933.

Olson D., Fadamiro H., Lundgren J., Heimpel G.E. 2000. Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol. Entomol. 25 (1): 17–26.

Ortel J. 1991. Effects of lead and cadmium on chemical composition and total water content of the pupal parasitoid, Pimpla turionellae. Entomol. Exp. Appl. 59 (1): 93–100.

Ortel J. 1996. Metal‐supplemented diets alter carbohydrate levels in tissue and hemolymph of gypsy moth larvae (Lymantria dispar, Lymantriidae, Lepidoptera). Environ. Toxicol. Chem. 15 (7): 1171–1176.

Parizanganeh A., Hajisoltani P., Zamani A. 2010. Concentration, distribution and comparison of total and bioavailable metals in top soils and plants accumulation in Zanjan Zinc Industrial Town-Iran. Procedia Environ. Sci. 2: 167–174.

Richmond W. 1973. Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin. Chem. 19 (12): 1350–1356.

Rifai N., Bachorik P.S., Albers J.J. 1999. Lipids, lipoproteins and apolipoproteins. p. 809–861. In: “Tietz Textbook of Clinical Chemistry”. 3rd ed. (C.A. Burtis, E.R. Ashwood, eds.). W.B. Saunders Company, Philadelphia, USA, 2256 pp.

Ryan R.O., Van Der Horst D.J. 2000. Lipid transport biochemistry and its role in energy production. Annu. Rev. Entomol. 45 (1): 233–260.

SAS Institute 1997. SAS/STAT User`s Guide for Personal Computers, SAS Institute, Cary NC, 18 pp.

Schmidt G.H., Ibrahim N.M., Abdallah M.D. 1992. Long-term effects of heavy metals in food on developmental stages of Aiolopus thalassinus (Saltatoria: Acrididae). Arch. Environ. Contam. Toxicol. 23 (3): 375–382.

Sharma R.K., Agrawal M. 2005. Biological effects of heavy metals: an overview. J. Environ. Biol. 26 (Suppl. 2): 301–313.

Shin B.S., Lee C.U. 2001. Effects of cadmium on total lipid content and fatty acids of the greater wax moth, Galleria mellonella. J. Ecol. Environ. 24 (6): 349–352.

Shorey H., Hale R. 1965. Mass-rearing of the larvae of nine noctuid species on a simple artificial medium. J. Econ. Entomol. 58 (3): 522–524.

Sildanchandra W., Crane M. 2000. Influence of sexual dimorphism in Chironomus riparius Meigen on toxic effects of cadmium. Environ. Toxicol. Chem. 19 (9): 2309–2313.

Srinivasan R., Uthamasamy S. 2005. Studies to elucidate antibiosis resistance in selected tomato accessions against fruit worm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Resis. Pest Manag. Newslett. 14 (2): 24–25.

Sun H.X., Dang Z., Xia Q., Tang W.C., Zhang G.R. 2011. The effect of dietary nickel on the immune responses of Spodoptera litura Fabricius larvae. J. Insect Physiol. 57 (7): 954–961.

Tarek M.Y.E., Fouda M.A., Hassan M.I., Abd-Elghaphar A.A., Hasaballah A.I. 2010. Toxicological effects of some heavy metal ions on Culex pipiens L. (Diptera: Culicidae). Egypt Acad. J. Biol. Sci. 2 (1): 63–76.

Tian X.P., Lu Y.M. 2009. On bio-availability of Fe, Mn, Cu and Zn in albic soil of the three river plain. Soils 41 (2): 196–200. Van Handel E. 1965. Estimation of glycogen in small amounts of tissue. Anal. Biochem. 11 (2): 256–265.

Van Ooik T., Rantala M.J., Saloniemi I. 2007. Diet-mediated effects of heavy metal pollution on growth and immune response in the geometrid moth Epirrita autumnata. Environ. Pollut. 145 (1): 348–354.

Waldbauer G. 1968. The consumption and utilization of food by insects. Adv. Insect Physiol. 5: 229–288.

Warrington S. 1987. Relationship between SO2 dose and growth of the pea aphid, Acyrthosiphon pisum, on peas. Environ. Pollut. 43 (2): 155–162.

Wu G.X., Ye G.Y., Hu C., Cheng J.A. 2006. Accumulation of cadmium and its effects on growth, development and hemolymph biochemical compositions in Boettcherisca peregrina larvae (Diptera: Sarcophagidae). Insect Sci. 13 (1): 31–39.

Yazdani E., Jalali Sendi J., Aliakbar A., Senthil-Nathan S. 2013. Effect of Lavandula angustifolia essential oil against lesser mulberry pyralid Glyphodes pyloalis Walker (Lep.: Pyralidae) and identification of its major derivatives. Pestic. Biochem. Physiol. 107 (2): 250–257.

Yazdani E., Jalali Sendi J., Hajizadeh J. 2014. Effect of Thymus vulgaris L. and Origanum vulgare L. essential oils on toxicity, food consumption, and biochemical properties of lesser mulberry pyralid Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). J. Plant Prot. Res. 54 (1): 53–61.

Zan S.T., Yang R.Y., Wang W.W. 2011. The correlation of soil physicochemical properties and copper-zinc accumulation of Elsholtzia splendens. J. Biol. 28: 46–49.

Journal of Plant Protection Research

The Journal of Polish Society of Plant Protection, Committee of Plant Protection; Polish Academy of Sciences, Institute of Plant Protection – National Research Institute

Journal Information

CiteScore 2016: 0.84

SCImago Journal Rank (SJR) 2016: 0.332
Source Normalized Impact per Paper (SNIP) 2016: 0.829

Cited By


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 64 64 13
PDF Downloads 26 26 4