Skip to main content

Advertisement

SpringerLink
Log in

Cadmium effects on the fitness-related traits and antioxidative defense of Lymantria dispar L. larvae

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Cadmium, like many other pollutants, is nondegradable and can be accumulated by Lymantria dispar at a level that affects fitness components, physiology, and development, which could indicate presence of environment pollution by heavy metals. The cadmium effect on fitness-related traits in the third, fourth, fifth, and sixth instar of L. dispar L. was determined. Furthermore, activities of the following antioxidative defense components after the larvae had been fed on the artificial cadmium-supplemented diet (50 μg Cd/g dry food) were assessed: superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APOX), total glutathione amount (GSH), glutathione-S-transferase (GST), glutathione reductase (GR), and the amount of free sulfhydryl (SH) groups. Statistically significant delay of development in the fourth, fifth, and sixth instar and decrease of the larval mass in the third and fourth instar were estimated after the exposure to cadmium through food in comparison to the control. There were no changes in SOD activity of cadmium-treated larvae. Significantly lower CAT, APOX, and GR activities were recorded in the third, fifth, and in the third instar, respectively. At the same time, higher activity was recorded in the sixth instar, while GST activity was higher in the third. GSH content was significantly lower during all instars after treatment but the amount of SH groups was higher in older larvae. The strategy of antioxidative defense and the adjustment or modulation of fitness-related traits in presence of cadmium was dependent on the age of larvae in L. dispar, which might be used in early metal risk assessment in Lepidoptera and other insects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahmad S (1992) Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects. Biochem Syst Ecol 20:269–296

    Article  CAS  Google Scholar 

  • Ahmad S (1995) Antioxidant mechanisms of enzymes and proteins. In: Ahmad S (ed) Oxidative stress and antioxidant defenses in biology. Chapman & Hall, New York, pp 238–272

    Chapter  Google Scholar 

  • Ahmad S, Pardini RS (1990) Mechanisms for regulating oxygen toxicity in phytophagous insects. Free Radic Biol Med 8:401–413

    Article  CAS  Google Scholar 

  • Badisa VL, Latinwo LM, Odewumi CO (2007) Mechanism of DNA damage by cadmium and interplay of antioxidant enzymes and agents. Environ Toxicol 22(2):144–151

    Article  CAS  Google Scholar 

  • Beutler E (1982) Catalase. In: Beutler E (ed) Red cell metabolism, a manual of biochemical methods. Grune and Stratton, Philadelphia, pp 105–106

    Google Scholar 

  • Blagojević DP, Grubor-Lajšić G (2000) Multifunctionality of antioxidant system in insects. Arch Biol Sci 52(4):185–194

    Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye bending. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Canesi L, Ciacci C, Betti M, Malatesta M, Gazzanelli G, Gallo G (1999) Growth factors stimulate the activity of key glycolytic enzymes in isolated digestive gland cells from mussels (Mytilus galloprovincialis Lam.) through tyrosine kinase-mediated signal transduction. Gen Comp Endocrinol 116:241–248

    Article  CAS  Google Scholar 

  • Cervera A, Maymo AC, Martinez-Pardo R, Garcera MD (2003) Antioxidant enzymes in Oncopeltus fasciatus (Heteroptera: Lygaeidae) exposed to cadmium. Physiol Ecol 32(4):705–710

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chaney RL, Ryan JA, Li Y-M, Brown SL (1999) Soil cadmium as a threat to human health. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Kluwer, Dordrecht, pp 219–256

    Chapter  Google Scholar 

  • Chinni S, Yallapragda PR (2000) Toxicity of copper, cadmium, zinc and lead to Penaeus indicus postlarvae: effects of individual metals. J Environ Biol 21(3):255–258

    CAS  Google Scholar 

  • Dallinger R, Rainbow PS (1991) Ecotoxicology of metals in invertebrates. SETAC-Europe Conference, Sheffield, England. Lewis, Boca Raton, pp 461

  • Devkota B, Schmidt GH (2000a) Accumulation of heavy metals in grass and grasshoppers from the Taigetos Mountains, Greece. Agric Ecosyst Environ 78:85–91

    Article  CAS  Google Scholar 

  • Devkota B, Schmidt GH (2000b) Life span and fecundity of Aiolopus thalassinus exposed to dietary heavy metals (Hg, Cd, Pb). Boll Zool Agr Bachic II 32(2):119–134

    Google Scholar 

  • Ellman CL (1959) Tissue sulfhydril groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29:187–197

    Article  CAS  Google Scholar 

  • Filipić M, Fatur T, Vudrag M (2006) Molecular mechanisms of cadmium induced mutagenicity. Hum Exp Toxicol 25:67–77

    Article  Google Scholar 

  • Fornazier RF, Ferreira RR, Pereira GJG, Molina SMG, Smith RJ, Lea PJ, Azavedo RA (2002) Cadmium stress in sugar cane callus cultures: effect on antioxidant enzymes. Plant Cell Tissue Organ Cult 71:125–131

    Article  CAS  Google Scholar 

  • Ginterneiter S, Ortel J, Nopp HJ (1993) Bioaccumulation of cadmium, lead, copper, and zinc in successive developmental stages of Lymantria dispar L. (Lymantriidae, Lepid.)—a life cycle study. Arch Environ Contam Toxicol 25:55–61

    Google Scholar 

  • Glatzle D, Vuilleumier JP, Weber F, Decker K (1974) Glutathione reductase test with whole blood: a convenient procedure for assessment of the riboflavin status in humans. Exp 30:565–638

    Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2 vinyl pyridine. Anal Biochem 106:207–212

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Gluthatione-S-transferases. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, New York

    Google Scholar 

  • Heliovaara K, Vaisanen R (1990) Heavy-metal contents in pupae of Bupalus piniarius (Lepidoptera: Geometridae) and Panolis flammea (Lepidoptera: Noctuidae) near an industrial source. Environ Entomol 19:481–485

    CAS  Google Scholar 

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  • Ilijin L, Perić Matruga 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 58(1–2):91–99

    Article  CAS  Google Scholar 

  • Irons RD, Sawahata R (1985) Phenols, catechols, and quinines. In: Anders MW (ed) Bioactivation of foreign compounds. Academic, San Diego, pp 259–279

    Google Scholar 

  • Ivanović J, Janković-Hladni M (1991) Hormones and metabolism in insect stress. CRC, Boca Raton

    Google Scholar 

  • Jovanović-Galović A, Blagojević D, Grubor-Lajšić G, Worland R, Spasić MB (2004) Role of antioxidant defense during different stages of preadult life cycle in European corn borer (Ostrinia nubilalis, Hubn.): diapause and metamorphosis. Arch Insect Biochem Physiol 55:79–89

    Article  Google Scholar 

  • Knežević J (2004) Analysis of pollutant contents in the air and precipitation—EMEP Station Kamenički Vis. In: Kadović R and Knezević M (eds) Forest condition monitoring in the Republic of Serbia, Annual Report ICP Forest 2003, Level I. Minist Sci Environ Prot Serb, FineGRAF.

  • Korsloot A, Van Gestel CAM, Van Straalen NM (2004) Environmental stress and cellular response in arthropods. CRC, Boca Raton

    Google Scholar 

  • Lance DR (1983) Host-seeking behavior of the gypsy moth: the influence of polyphagy and highly apparent host plants. In: Ahmad S (ed) Herbivorous insects: host-seeking behavior and mechanisms. Academic, New York, pp 210–224

    Google Scholar 

  • Lauverjat S, Ballan-Dufrancias C, Wegnez M (1989) Detoxification of cadmium. Ultrastructural study and electron-microprobe analysis of the midgut in a cadmium-resistant strain of Drosophila melanogaster. Biol Met 2:97–107

    Article  CAS  Google Scholar 

  • Li LJ, Liu XM, Duan YH, Guo YP, Cheng B, Guo J, Xi YY, Ma EB (2006) Accumulation of cadmium and copper by female Oxya chinensis (Orthopteta: Acridoidae) in soil–plant–insect system. J Environ Sci 18(2):341–346

    CAS  Google Scholar 

  • Maryanski M, Kramartz P, Lakowski R, Niklinska M (2002) Decreased energetic reserves, morphological changes and accumulation of metals in carabid bettles (Poecilus cupreus L.) exposed to zinc- or cadmium-contaminated food. Ecotoxicol 11:127–139

    Article  CAS  Google Scholar 

  • Mathews MC, Summers CB, Felton GW (1997) Ascorbate peroxidase: a novel antioxidant enzyme in insects. Arch Insect Biochem Pharm 34:57–68

    Article  CAS  Google Scholar 

  • McChaton CP, Pascoe D (1991) Brief exposure of first and fourth instar Chironomus riparius larvae to equivalent assumed doses of cadmium: effects on adult emergence. Water Air Soil Poll 60:395–403

    Article  Google Scholar 

  • Migula P, Laszczyca P, Augustyniak M, Wilczek G, Rozpedek K, Kafel A, Woloszyn M (2004) Antioxidative defence enzymes in beetles from a metal pollution gradient. Biol Bratisl 59(5):645–654

    CAS  Google Scholar 

  • Mirčić D, Janković-Tomanić MZ, Nenadović VA, Franeta F, Lazarević JM (2010) The effects of cadmium on the life history traits of Lymantria dispar L. Arch Biol Sci 62(4):1013–1020

    Article  Google Scholar 

  • Mistra HP, Fridovich I (1972) The role of superoxide anion in the antioxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    Google Scholar 

  • Mouneyrac C, Leving PTY, Leung MY (2011) Cost of tolerance. In: Triquet CA, Rainbow PS, Romeo M (eds) Tolerance to environmental contaminants. CRC, Taylor & Francis Group, Boca Raton

    Google Scholar 

  • Niu C-Y, Jiang Y, Lei C-L, Hu C (2002) Effects of cadmium on housefly: influence on growth and development and metabolism during metamorphosis of housefly. Entomol Sin 9(1):27–33

    Google Scholar 

  • Nursita AI, Singh B, Less E (2005) The effects of cadmium, copper, lead, and zinc on the growth and reproduction of Proisotoma minuta Tullberg (Collembola). Ecotoxicol Environ Saf 60:306–314

    Article  CAS  Google Scholar 

  • Odell TM, Bell RA, Mastro VC, Tanner JA, Kennedy JF (1984) Production of the gypsy moth Lymantria dispar for research and biological control. In: King EG, Leppla NC (eds) Advances and challenges in insect rearing. USDA-ARS, New Orleans, pp 156–166

    Google Scholar 

  • Ortel J (1995) Changes in protein content and free amino acid composition in metalo-contaminated gypsy moth larvae (Lymantria dispar L., Lymantriidae, Lepidoptera). Comp Biochem Physiol C 112:291–298

    CAS  Google Scholar 

  • Pedersen SA, Kristiansen E, Andersen RA, Zachariassen KE (2008) Cadmium is deposited in the gut content of larvae of the beetle Tenebrio molitor and involves a Cd-binding protein of the low cysteine type. Comp Biochem Physiol C 148:217–222

    CAS  Google Scholar 

  • Perić Mataruga V, Janković-Hladni M, Ivanović J (1988) The effect of different feeding substrates on the development of Lymantria dispar L. Plant Protect 39:39–45

    Google Scholar 

  • Perić-Mataruga V, Blagojević D, Spasić MB, Ivanović J, Janković-Hladni M (1997) Effect of the host plant on the antioxidative defence in the midgut of Lymantria dispar L. caterpillars of different population origins. J Insect Physiol 43(1):101–106

    Article  Google Scholar 

  • Pickett CB, Lu AYH (1989) Glutathione-S-transferases: gene structure, regulation and biological function. Annu Rev Biochem 58:743–764

    Article  CAS  Google Scholar 

  • Rayms-Keller A, Olson KE, McGaw M, Oray C, Carlson JO, Beaty BJ (1998) Effect of heavy metals on Aedes aegypti (Diptera: Culicidae) larvae. Ecotoxicol Environ Saf 39:41–47

    Article  CAS  Google Scholar 

  • Rayms-Keller A, McGaw M, Oray C, Carlson JO, Beaty BJ (2000) Molecular cloning and characterization of a metal responsive Aedes aegypti intestinal mucin Cdna. Insect Mol Biol 9:419–426

    Article  CAS  Google Scholar 

  • Saint-Denis M, Narbonne JF, Arnaud C, Ribera D (2001) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of lead acetate. Soil Biol Biochem 33:395–404

    Article  CAS  Google Scholar 

  • Schmidt GH, Ibrahim NMM, Abdallah MD (1991) Toxological studies on the long- term effects of heavy metals (Hg, Cd, Pb) in soil on the development stages of Aiolopus thalassinus (Saltatoria: Acrididae). Arch Environ 107:109–134

    CAS  Google Scholar 

  • Shacter E (2000) Quantification and significance of protein oxidation in biological samples. Drug Met Rev 32:302–326

    Article  Google Scholar 

  • Smith J, Shrift A (1979) Phylogenetic distribution of gluthatione peroxidase. Comp Biochem Physiol 63B:39–44

    CAS  Google Scholar 

  • Sohal RS, Allen RG, Orr WC (1990) Effect of age on superoxide dismutase, catalase, glutathione reductase, inorganic peroxides, TBA-reactive material, GSH/GSSG, NADPH/NADP+, and NADH/NAD+ in Drosophila melanogaster. Mech Ageing Dev 56:223–235

    Article  CAS  Google Scholar 

  • Sokal RS, Rohlf FJ (1981) Biometry. Freeman, San Francisco

    Google Scholar 

  • The SAS Institute (2003) SAS 9.1.3. Service Pack 4, Cary, NC, USA

  • US Environmental Protection Agency (1991) Water quality criteria summary list. USEPA, Washington

    Google Scholar 

  • Vlahogianni T, Dassenakis M, Scoullos MJ, Valavanidis A (2007) Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals pollution in coastal areas from the Saronikos Gulf of Greece. Mar Pollut Bull 54:1361–1371

    Article  CAS  Google Scholar 

  • Vlahović M, Ilijin L, Lazarević J (2001) Acute effect of cadmium on larval growth of Lymantria dispar L. Ekol 36:131–137

    Google Scholar 

  • Vlahović M, Lazarević J, Perić-Mataruga V, Ilijin L, Mrdaković M (2008) Plastic responses of larval mass and alkaline phosphatase to cadmium in the gypsy moth larvae. Ecotoxicol Environ Saf 72:1148–1155

    Article  Google Scholar 

  • Vlahović M, Perić-Mataruga V, Ilijin L, Mrdaković M, Mirčić D, Todorović D, Lazarević J (2012) Changes in activity of non-specific esterases in cadmium treated Lymantria dispar larvae. Ecotoxicol 21:370–378

    Article  Google Scholar 

  • Wang Y, Fang J, Leonard SS, Rao KM (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443

    Article  CAS  Google Scholar 

  • Wilczek G, Babczynska A, Augustyniak M, Migula P (2004) Relations between metals (Zn, Pb, Cd, and Cu) and glutathione- dependent detoxifying enzymes in spiders from a heavy metal pollution gradient. Environ Pollut 132:453–461

    Article  CAS  Google Scholar 

  • Wu GX, Ye GY, Hu C, Cheng JA (2006) Accumulation of cadmium and its effects on growth, development and hemolymph biochemical compositions in Boettcherisca peregrina larvae (Diptera: Sarcophagidae). Insect Sci 13:31–39

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Serbian Ministry of Education and Science (grant no.173027).

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, State University of Novi Pazar, Vuka Karadžića bb, 36 300, Novi Pazar, Serbia

    Dejan Mirčić

  2. Department of Insect Physiology and Biochemistry, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Despot Stefan Blvd. 142, 11060, Belgrade, Serbia

    Dejan Mirčić, Vesna Perić-Mataruga, Larisa Ilijin, Marija Mrdaković, Milena Vlahović & Jelica Lazarević

  3. Department of Physiology, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Despot Stefan Blvd. 142, 11060, Belgrade, Serbia

    Duško Blagojević

Authors
  1. Dejan Mirčić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duško Blagojević
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vesna Perić-Mataruga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Larisa Ilijin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marija Mrdaković
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Milena Vlahović
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jelica Lazarević
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dejan Mirčić.

Additional information

Responsible editor: Markus Hecker

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mirčić, D., Blagojević, D., Perić-Mataruga, V. et al. Cadmium effects on the fitness-related traits and antioxidative defense of Lymantria dispar L. larvae. Environ Sci Pollut Res 20, 209–218 (2013). https://doi.org/10.1007/s11356-012-1057-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-012-1057-z

Keywords

Search

Navigation