, Volume 23, Issue 5, pp 757–766 | Cite as

Response of Tribolium castaneum to elevated copper concentrations is influenced by history of metal exposure, sex-specific defences, and infection by the parasite Steinernema feltiae

  • Paulina E. KramarzEmail author
  • Anna Mordarska
  • Magdalena Mroczka


We studied how copper toxicity in the red flour beetle, Tribolium castaneum changed as a result of infection by the entomopathogenic nematode Steinernema feltiae. Measured traits were: respiration, growth and survival, as well as the concentrations of copper within beetle tissues and in its diet. By comparing F1 and F5 generation we were able to answer how long-term metal exposure changed the responses to both copper and the parasite. The beetles did accumulate copper; however, the results indicated that copper concentrations in beetle tissues were affected by nematode infection, the sex of the experimental animals, and the number of generations of exposure. Five generations of exposure to copper resulted in the highest dry body mass of infected beetles of both sexes; additionally, this group also had the lowest copper concentrations in their tissues. The only factor that had a significant effect on respiration was infection by nematodes: infected beetles of both sexes in both generational groups had significantly decreased respiration rates. Survival was lowest in nematode-infected animals of both sexes from both generations, regardless of exposure to copper. Our results confirm that an organism’s response to metal pollution is dependent on its health status and sex. We also found that the history of exposure to metal was equally important—we found enhanced resistance to copper intoxication after only five generations of exposure.


Pre-exposure Metal toxicity Parasite Energy budget Biological control 



We thank Patrycja Gibas for assistance in the laboratory. We also thank Lindsay Higgins for the text editing and her comments on the manuscript. The project was supported by Grant No. NN304 027334 from the State Committee For Scientific Research and Jagiellonian University (DS/WBINOZ/INOŚ/747).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Canli M (2006) Effects of copper pre-exposure routes on the energy reserves and subsequent copper toxicity in Daphnia magna. Environ Toxicol 21:521–527CrossRefGoogle Scholar
  2. Castillo JC, Reynolds SE, Eleftherianos I (2011) Insect immune responses to nematode parasites. Trends Parasitol 27:537–547CrossRefGoogle Scholar
  3. Donker MH, Zonneveld C, van Straalen NM (1993) Early reproduction and increased reproductive allocation in metal-adapted populations of the terrestrial isopod Porcellio scaber. Oecologia 96:316–323CrossRefGoogle Scholar
  4. Donker MH, Raedecker MH, van Straalen NM (1996) The role of zinc regulation in the zinc tolerance mechanism of the terrestrial isopod Porcellio scaber. J Appl Ecol 33:955–964CrossRefGoogle Scholar
  5. Fisker KV, Sorensen JG, Damgaard C, Pedersen KL, Holmstrup M (2011) Genetic adaptation of earthworms to copper pollution: is adaptation associated with fitness costs in Dendrobaena octaedra? Ecotoxicology 20:563–573CrossRefGoogle Scholar
  6. Gudbrandsen M, Line LE, Aamodt S, Stenersen J (2007) Short-term pre-exposure increases earthworm tolerance to mercury. Eur J Soil Biol 43:261–267CrossRefGoogle Scholar
  7. Hazir S, Kaya HK, Stock P, Keskun N (2003) Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turk J Biol 27:181–202Google Scholar
  8. Hoffmann AA, Parsons PA (1994) Evolutionary genetics and environmental stress. Oxford University Press, OxfordGoogle Scholar
  9. Holmstrup M, Petersen BF, Larsen MM (1998) Combined effects of copper, desiccation, and frost on the viability of earthworm cocoons. Environ Toxicol Chem 17:897–901CrossRefGoogle Scholar
  10. Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier Applied Science, BarkingGoogle Scholar
  11. Kadar E, Santos RS, Powell JJ (2006) Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vent sites of the Mid-Atlantic Ridge. Environ Res 101:221–229CrossRefGoogle Scholar
  12. Khan MAQ, Ahmed SA, Salazar A, Gurumendi J, Khan A, Vargas M, von Catalin B (2007) Effect of Temperature on heavy metal toxicity to earthworm Lumbricus terrestris (Annelida:Lumbricus Oligochaeta). EnvironToxicol 22:487–494Google Scholar
  13. Kramarz P, Laskowski R (1999) Toxicity and possible food-chain effects of copper, dimethoate and a detergent (LAS) on a centipede (Lithobius mutabilis) and its prey (Musca domestica). Appl Soil Ec 13:177–185CrossRefGoogle Scholar
  14. Kramarz P, Zwolak M, Laskowski R (2005) Effect of interaction between density dependence and toxicant exposure on population growth rate of the potworm Enchytraeus doerjesi. Environ Toxicol Chem 24:537–540CrossRefGoogle Scholar
  15. Kramarz PE, de Vaufleury A, Zygmunt PMS, Verdun C (2007) Increased response to cadmium and Bacillus thuringiensis maize toxicity in the snail Helix aspersa infected by the nematode Phasmarhabditis hermaphrodita. Environ Toxicol Chem 26:73–79CrossRefGoogle Scholar
  16. Minguez L, Boiche′ A, Sroda S, Mastitsky S, Brule N, Bouquerel J, Giamberini L (2012) Cross-effects of nickel contamination and parasitism on zebra mussel physiology. Ecotoxicology 21:538–547CrossRefGoogle Scholar
  17. Mirčić D, Janković-Tomanić M, Nenadović V, Franeta F, Lazarević J (2010) The effects of cadmium on the life history traits of Lymantria dispar l. Arch Biol Sci, Belgrade 62:1013–1020CrossRefGoogle Scholar
  18. Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM (2011) Non-immunological defense in an evolutionary framework. Trends Ecol Evol 26:242–248Google Scholar
  19. Paul-Pont I, Gonzalez P, Baudrimont M, Jude F, Raymond N, Bourrasseau L, Le Goïc N, Haynes F, Legeay A, Paillard C, de Montaudouin X (2010) Interactive effects of metal contamination and pathogenic organisms on the marine bivalve Cerastoderma edule. Mar Pollut Bull 60:515–525CrossRefGoogle Scholar
  20. Ramos-Rodrıquez O, Campbell JF, Ramaswamya SB (2006) Pathogenicity of three species of entomopathogenic nematodes to some major stored-product insect pests. J Stored Prod Res 42:241–252CrossRefGoogle Scholar
  21. Sandifer RD, Hopkin SP (1996) Effects of pH on the toxicity of cadmium, copper, lead and zinc to Folsomia candida Willem, 1902 (Collembola) in a standard laboratory test system. Chemosphere 33:2475–2486CrossRefGoogle Scholar
  22. Sildanchandra W, Crane M (2000) Influence of sexual dimorphism in Chironomus riparius meigen on toxic effects of cadmium. Ecotox Environ Safe 19:2309–2313Google Scholar
  23. Sokal RR, Rohlf FJ (1994) Biometry: the principles and practices of statistics in biological research. Freeman and Co., New YorkGoogle Scholar
  24. Stillwell RC, Blanckenhorn WU, Teder T, Davidowitz G, Fox CW (2010) sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu Rev Entomol 55:227–245CrossRefGoogle Scholar
  25. Van Lenteren JC (2011) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol. doi: 10.1007/s10526-011-9395-1 Google Scholar
  26. Zygmunt PMS, Maryanski M, Laskowski R (2006) Body mass and caloric value of the ground beetle (Pterostichus oblongopunctatus) (Coleoptera, Carabidae) along a gradient of heavy metal pollution. Environ Toxicol Chem 25:2709–2714CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Paulina E. Kramarz
    • 1
    Email author
  • Anna Mordarska
    • 1
  • Magdalena Mroczka
    • 1
  1. 1.Institute of Environmental SciencesJagiellonian UniversityKrakówPoland

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