Heavy metal exposure through artificial diet reduces growth and survival of Spodoptera litura (Lepidoptera: Noctuidae)

  • Sajjad AliEmail author
  • Muhammad Irfan Ullah
  • Muhammad Farhan SaeedEmail author
  • Samina Khalid
  • Muhammad Saqib
  • Muhammad Arshad
  • Muhammad Afzal
  • Christos A. DamalasEmail author
Research Article


Insect physiology is affected by the presence of toxins in the surrounding environment of insects as well as their food sources. The objective of this study was to determine the effect of heavy metal exposure to two low concentrations (50 μg/g and 150 μg/g) of lead (Pb) and zinc (Zn) through artificial diet to the larvae on biological parameters of Asian armyworm (Spodoptera litura Fabricius) (Lepidoptera: Noctuidae). Both Pb and Zn, even at low concentrations, had relatively high toxic effects on S. litura larvae (P < 0.01). S. litura larval weight and length suffered the maximum reduction when the larvae were fed on diet mixed with the high Pb concentration (150 μg/g) tested compared to the other treatments. At the same Pb concentration (150 μg/g), values of larva growth index, pupa growth index, immature growth index, standardized growth index, and fitness index were 4.66, 7.33, 7.82, 5.35, and 10.00 times lower, respectively, than those of control. At the same Zn concentration (150 μg/g), values of larval growth index, pupal growth index, immature growth index, standardized growth index, and fitness index were 5.61, 3.00, 3.04, 3.23, and 9.24 times lower, respectively, than those of control. The survival rate of S. litura larvae was also lower (12.5%) when the larvae were fed on diet mixed with Pb at 150 μg/g after 10 days of observation. Overall, the presence of those heavy metals in the environment, even at low concentrations, would exert an adverse impact on larvae development of this insect. From this point of view, findings could provide a basis for long-term evaluation of heavy metal risk and its impact on populations of important agricultural pests.


Asian armyworm Bioindicator Larvae Lead Pollution Stress Zinc 



  1. Ahmad M, Ghaffar A, Rafiq M (2013a) Host plants of leafworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in Pakistan. Asian J Agric Biol 1:23–28Google Scholar
  2. Ahmad K, Khan ZI, Jabeen H, Ashraf M, Shaheen M, Raza SH (2013b) Assessment of heavy metals and metalloids toxicity in buffaloes fed on forages irrigated with domestic wastewater in Bhalwal, Sargodha, Pakistan. Pakistan J Zool 45:1629–1637Google Scholar
  3. Al-Dhafar ZM, Sharaby A (2012) Effect of zinc sulfate against the red palm weevil Rhynchophorus ferrugineus with reference to their histological changes on the larval midgut and adult reproductive system. J Agric Sci Technol A2:888–900Google Scholar
  4. Atafar Z, Mesdaghinia A, Nouri J, Homaee M, Yunesian M, Ahmadimoghaddam M, Mahvi AH (2010) Effect of fertilizer application on soil heavy metal concentration. Environ Monit Assess 160:83–89CrossRefGoogle Scholar
  5. Augustyniak M, Juchimiuk J, Przybyłowicz WJ, Mesjasz-Przybyłowicz J, Babczyńska A, Migula P (2006) Zinc-induced DNA damage and the distribution of metals in the brain of grasshoppers by the comet assay and micro-PIXE. Comp Biochem Physiol C Toxicol Pharmacol 144:242–251CrossRefGoogle Scholar
  6. Azam I, Afsheen S, Zia A, Javed M, Saeed R, Sarwar MK, Munir B (2015) Evaluating insects as bioindicators of heavy metal contamination and accumulation near industrial area of Gujrat, Pakistan. Biomed Res Int 2015:942751CrossRefGoogle Scholar
  7. Baghban A, Sendi JJ, Zibaee A, Khosravi R (2014) Effect of heavy metals (Cd, Cu, and Zn) on feeding indices and energy reserves of the cotton bollworm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). J Plant Prot Res 54:367–373Google Scholar
  8. Bahadorani S, Hilliker AJ (2009) Biological and behavioral effects of heavy metals in Drosophila melanogaster adults and larvae. J Insect Behav 22:399–411CrossRefGoogle Scholar
  9. Behmer ST, Lloyd CM, Raubenheimer D, Stewart-Clark J, Knight J, Leighton RS, Harper FA, Smith JAC (2005) Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Funct Ecol 19:55–66CrossRefGoogle Scholar
  10. Campbell AJ, Biesmeijer JC, Varma V, Wäckers FL (2012) Realising multiple ecosystem services based on the response of three beneficial insect groups to floral traits and trait diversity. Basic Appl Ecol 13:363–370CrossRefGoogle Scholar
  11. Cock J, Yoshida S, Forno DA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, ManilaGoogle Scholar
  12. Coleman CM, Boyd RS, Eubanks MD (2005) Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. J Chem Ecol 31:1669–1681CrossRefGoogle Scholar
  13. Eesa NM, El-Sherif H, El-Sayed WM, Abd El-Monem DH (2017) Bioefficacy of cadmium and lead on cotton leafworm Spodoptera littoralis (Lepidoptera: Noctuidae) larvae. Inv Reprod Dev 61:27–33CrossRefGoogle Scholar
  14. Fajer ED, Bowers MD, Bazzaz FA (1989) The effects of enriched carbon dioxide atmospheres on plant-insect herbivore interactions. Science 243:1198–1201CrossRefGoogle Scholar
  15. Fisher BL (1998) Insect behavior and ecology in conservation: preserving functional species interactions. Ann Entom Soc Am 91:155–158CrossRefGoogle Scholar
  16. Gao C, Bei Y, Chen T, Gu X (2004) On factors causing the outbreak of Spodoptera litura (Fabricius). Acta Agric Univ Zhejiangensis 16:332–335Google Scholar
  17. Gimeno-García E, Andreu V, Boluda R (1996) Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environ Pollut 92:19–25CrossRefGoogle Scholar
  18. Hamzeh MA, Aftabi A, Mirzaee M (2011) Assessing geochemical influence of traffic and other vehicle-related activities on heavy metal contamination in urban soils of Kerman city, using a GIS-based approach. Environ Geochem Health 33:577–594CrossRefGoogle Scholar
  19. Haq R, Farhanullah Khan M, Haq E (2011) Adverse effect of lead acetate on Drosophila melanogaster. J Basic Appl Sci 7:157–163CrossRefGoogle Scholar
  20. Heliövaara K, Väisänen R (1990) Heavy-metal contents in pupae of Bupalus piniarius (Lepidoptera: Geometridae) and Panolis flammea (Lepidoptera: Noctuidae) near an industrial source. Environ Entomol 19:481–485CrossRefGoogle Scholar
  21. 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 105:288–294CrossRefGoogle Scholar
  22. Itoyama K, Kawahira Y, Murata M, Tojo S (1999) Fluctuations of some characteristics in the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae) reared under different diets. Appl Entomol Zool 34:315–321CrossRefGoogle Scholar
  23. Jeantet AY, Ballan-Dufrancais C, Martoja R (1977) Insects resistance to mineral pollution. Importance of spherocrystal in ionic regulation. Rev Ecol Biol Sol 14:563–582Google Scholar
  24. Jhee EM, Boyd RS, Eubanks MD (2006) Effectiveness of metal-metal and metal-organic compound combinations against Plutella xylostella: implications for plant elemental defense. J Chem Ecol 32:239–259CrossRefGoogle Scholar
  25. Kafel A, Rozpedek K, Szulińska E, Zawisza-Raszka A, Migula P (2014) The effects of cadmium or zinc multigenerational exposure on metal tolerance of Spodoptera exigua (Lepidoptera: Noctuidae). Environ Sci Pollut Res 21:4705–4715CrossRefGoogle Scholar
  26. Kazemi-Dinan A, Thomaschky S, Stein RJ, Krämer U, Müller C (2014) Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol 202:628–639CrossRefGoogle Scholar
  27. Lapointe SL, Weathersbee AA III, Doostdar H, Mayer RT (2004) Effect of dietary copper on larval development of Diaprepes abbreviatus (Coleoptera: Curculionidae). Florida Entomol 87:25–29CrossRefGoogle Scholar
  28. Leonard SS, Harris GK, Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Radic Biol Med 37:1921–1942CrossRefGoogle Scholar
  29. Liu Y, Su C, Zhang H, Li X, Pei J (2014) Interaction of soil heavy metal pollution with industrialisation and the landscape pattern in Taiyuan city, China. PLoS One 9:e105798CrossRefGoogle Scholar
  30. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
  31. Maret W (2005) Zinc coordination environments in proteins determine zinc functions. J Trace Elem Med Biol 19:7–12CrossRefGoogle Scholar
  32. Marschner H (1983) General introduction to the mineral nutrition of plants. In: Lauchii A, Bieleskir L (eds) Inorganic plant nutrition. Springer Verlag, New York, pp 5–60CrossRefGoogle Scholar
  33. Martoja R, Bouquegneau JM, Verthe C (1983) Toxicological effects and storage of cadmium and mercury in an insect Locusta migratoria (Orthoptera). J Invert Pathol 42:17–32CrossRefGoogle Scholar
  34. Muchuweti M, Birkett JW, Chinyanga E, Zvauya R, Scrimshaw MD, Lester JN (2006) The heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: implications for human health. Agric Ecosyst Environ 112:41–48CrossRefGoogle Scholar
  35. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  36. Nummelin M, Lodenius M, Tulisalo E, Hirvonen H, Alanko T (2007) Predatory insects as bioindicators of heavy metal pollution. Environ Pollut 145:339–347CrossRefGoogle Scholar
  37. Page V, Feller U (2015) Heavy metals in crop plants: transport and redistribution processes on the whole plant level. Agronomy 5:447–463CrossRefGoogle Scholar
  38. Parven N, Bashar MA, Quraishi SB (2009) Bioaccumulation of heavy and essential metals in trophic levels of the pond ecosystem. J Bangladesh Acad Sci 33:131–138CrossRefGoogle Scholar
  39. Popham HJ, Shelby KS (2006) Uptake of dietary micronutrients from artificial diets by larval Heliothis virescens. J Insect Physiol 52:771–777CrossRefGoogle Scholar
  40. Pretorius LM (1976) Laboratory studies on the development and reproductive performance of Heliothis armigera (Hubn.) on various food plants. J Entomol Soc South Afr 39:337–343Google Scholar
  41. Qadir A, Malik RN (2009) Assessment of an index of biological integrity (IBI) to quantify the quality of two tributaries of river Chenab, Sialkot, Pakistan. Hydrobiologia 621:127–153CrossRefGoogle Scholar
  42. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65CrossRefGoogle Scholar
  43. Safaee S, Fereidoni M, Mahdavi-Shahri N, Haddad F (2014) Effects of lead on the development of Drosophila melanogaster. Period Biol 116:259–265Google Scholar
  44. Saleem MA, Ahmad M, Ahmad M, Aslam M, Sayyed AH (2008) Resistance to selected organochlorine, organophosphate, carbamates and pyrethroid insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. J Econ Entomol 101:1667–1675CrossRefGoogle Scholar
  45. Seth RK, Sharma VP (2002) Growth, development, reproductive competence and adult behaviour of Spodoptera litura (Lepidoptera: Noctuidae) reared on different diets. In: Bloem S, Carpenter JE, Hendrichs J (eds) Evaluation of Lepidoptera population suppression by radiation induced sterility. IAEA-TECDOC-1283, Vienna, pp 15–28Google Scholar
  46. Sharaby A, EL-Hawari F, Ibrahim SA (2011) Some inorganic salts for production of sterile adults of the red palm weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae). J Agric Sci Technol 1:728–733Google Scholar
  47. Sharma RK, Agrawal M, Marshall F (2006) Heavy metal contamination in vegetables grown in wastewater irrigated areas of Varanasi, India. Bull Environ Contam Toxicol 77:312–318CrossRefGoogle Scholar
  48. Sharma RK, Agrawal M, Marshall FM (2008) Heavy metal (Cu, Zn, Cd and Pb) contamination of vegetables in urban India: a case study in Varanasi. Environ Pollut 154:254–263CrossRefGoogle Scholar
  49. Shirley MD, Sibly RM (1999) Genetic basis of a between-environment trade-off involving resistance to cadmium in Drosophila melanogaster. Evolution 53:826–836CrossRefGoogle Scholar
  50. Shu Y, Gao Y, Sun H, Zou Z, Zhou Q, Zhang G (2009) Effects of zinc exposure on the reproduction of Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Ecotoxicol Environ Saf 72:2130–2136CrossRefGoogle Scholar
  51. Shu Y-H, Du Y, Wang J-W (2012a) Effects of lead stress on the growth and reproduction of Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Chin J Appl Ecol 23:1562–1568Google Scholar
  52. Shu Y, Zhang G, Wang J (2012b) Response of the common cutworm Spodoptera litura to zinc stress: Zn accumulation, metallothionein and cell ultrastructure of the midgut. Sci Total Environ 438:210–217CrossRefGoogle Scholar
  53. Sorsa M, Pfeifer S (1973) Effects of cadmium on development time and prepupal puffing pattern of Drosophila melanogaster. Hereditas 75:273–277CrossRefGoogle Scholar
  54. Stolpe C, Müller C (2016) Effects of single and combined heavy metals and their chelators on aphid performance and preferences. Environ Toxicol Chem 35:3023–3030CrossRefGoogle Scholar
  55. Sun H, Shu Y, Tang W, Wang Q, Zhou Q, Zhang G (2007) Nickel accumulation and its effects on the survival rate of Spodoptera litura Fabricius under continuous nickel stress. Chin Sci Bull 52:1957–1963CrossRefGoogle Scholar
  56. Sun HX, Zhou Q, Tang WC, Shu YH, Zhang GR (2008) Effects of dietary nickel on detoxification enzyme activities in the midgut of Spodoptera litura Fabricius larvae. Chin Sci Bull 53:3324–3330Google Scholar
  57. Sun HX, Xia Q, Tang WC, Zhou Q, Zhang GR, Dang Z (2010) Effects of dietary nickel on apoptosis of hemocytes of Spodoptera litura (Fabricius) larvae. Chin Sci Bull 55:390–397CrossRefGoogle Scholar
  58. Tariq SR, Shafiq M, Chotana GA (2016) Distribution of heavy metals in the soils associated with the commonly used pesticides in cotton fields. Scientifica 2016:7575239CrossRefGoogle Scholar
  59. Verkleij JA (1993) The effects of heavy metal stress on higher plants and their use as biomonitors. Plant as bioindicators: indicators of heavy metals in the terrestrial environment. VCH, New York, pp 415–424Google Scholar
  60. Vickerman DB, Young JK, Trumble JT (2002) Effect of selenium-treated alfalfa on development, survival, feeding and oviposition preferences of Spodoptera exigua (Lepidoptera: Noctuidae). Environ Entomol 31:953–959Google Scholar
  61. Xia Q, Sun H, Hu X, Shu Y, Gu D, Zhang G (2005) Apoptosis of Spodoptera litura larval hemocytes induced by heavy metal zinc. Chin Sci Bull 50:2856–2860CrossRefGoogle Scholar
  62. Xia Q, Hu X, Shu Y, Sun H, Zhang G, Gu D (2006) Survival and development of | sl Microplitis bicoloratus Chen on larvae of Spodoptera litura Fabricius stressed by heavy metal zinc. Acta Entomol Sin 49:387–392Google Scholar
  63. Xu Y, Tang H, Liu T, Li Y, Huang X, Pi J (2018) Effects of long-term fertilization practices on heavy metal cadmium accumulation in the surface soil and rice plants of double-cropping rice system in Southern China. Environ Sci Pollut Res 25:19836–19844CrossRefGoogle Scholar
  64. Ying-Hua S, Yan D, Jian-Wu W (2012) Effects of lead stress on the growth and reproduction of Spodoptera litura Fabricius (Lepidoptera: Noctuidae). J Appl Ecol 23:1562–1568 (in Chinese with English abstract)Google Scholar
  65. Zhao S, Qiu S, He P (2018) Changes of heavy metals in soil and wheat grain under long-term environmental impact and fertilization practices in North China. J Plant Nutr 41:1970–1979CrossRefGoogle Scholar
  66. Zvereva E, Serebrov V, Glupov V (2003) Activity and heavy metal resistance of non specific esterases in leaf beetle, Chrysomela lapponica from polluted and unpolluted habitats. Comp Biochem Physiol C Toxicol Pharmacol 135:383–391CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sajjad Ali
    • 1
    Email author
  • Muhammad Irfan Ullah
    • 2
  • Muhammad Farhan Saeed
    • 3
    Email author
  • Samina Khalid
    • 3
  • Muhammad Saqib
    • 2
  • Muhammad Arshad
    • 2
  • Muhammad Afzal
    • 2
  • Christos A. Damalas
    • 4
    Email author
  1. 1.Department of Entomology, UCA & ESThe Islamia University of BahawalpurBahawalpurPakistan
  2. 2.Department of Entomology, College of AgricultureUniversity of SargodhaSargodhaPakistan
  3. 3.Department of Environmental SciencesCOMSATS UniversityVehariPakistan
  4. 4.Department of Agricultural DevelopmentDemocritus University of ThraceOrestiadaGreece

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