Abstract
All processes involved in metal homeostasis must be coordinated to provide sufficient, but not toxic, concentrations of important bioelements, and to minimize detrimental effects of toxic metals. Our previous studies dealing with the exposure of O. nubilalis non-diapausing larvae to dietary Cd demonstrated that exposure to higher concentrations of Cd caused delay in the development of larvae, induced oxidative stress and also induced defense mechanisms against the toxic effects of Cd. The aim of the present study was to evaluate how acute and chronic exposure of O. nubilalis larvae to increased concentrations of dietary Cd affected the balance of important bioelements. The concentration of bioelements was analyzed in larvae (after short-term exposure) and pupae (after long-term exposure). The short-term exposure of final instar larvae (L5) to Cd did not affect significantly the concentration of any of the analyzed bioelements, while the long-term exposure of developing larvae to higher concentrations of Cd caused increase in the concentrations of Ca, Mg and Na in pupae. The bioaccumulation factor, calculated for bioelements after long-term exposure to Cd, was higher for the most bioelements in groups fed with diet containing higher concentrations of Cd, except K which displayed the opposite trend. Pearson correlation coefficient showed positive correlations between Cd and Ca, Mg, Na, Fe, Cu and Zn, while negative correlation was observed between Cd and K. The results indicate that impact on the balance of important bioelements might be one of the mechanisms of cadmium toxicity and certainly raise numerous questions for future research.
Similar content being viewed by others
References
Augustyniak M, Babczynska A, Augustyniak M (2009) Does the grasshopper Chorthippus brunneus adapt to metal polluted habitats? A study of glutathione-dependent enzymes in grasshopper nymphs. Insect Sci 16:33–42. https://doi.org/10.1111/j.1744-7917.2009.00251.x
Augustyniak M, Migula P (2000) Body burden with metals and detoxifying abilities of the grasshopper—Chorthippus brunneus (Thunberg) from industrially polluted areas. In: Markert B, Friese K (eds) Trace metals in the environment, Vol. 4. Trace elements—their distribution and effects in the environment. Elsevier, Amsterdam, pp 423–454. https://doi.org/10.1016/S0927-5215(00)80019-3
Avramov M, Schád É, Révész Á, Turiák L, Uzelac I, Tantos Á, Drahos L, Popović ŽD (2022) Identification of intrinsically disordered proteins and regions in a non-model insect species Ostrinia nubilalis (Hbn.). Biomolecules 12(4): 592. https://doi.org/10.3390/biom12040592
Ballan-Dufrançais C (2002) Localization of metals in cells of pterygote insects. Microsc Res Techniq 56:403–420. https://doi.org/10.1002/jemt.10041
Béchard KM, Gills PL, Wood CM (2008) Acute toxicity of waterborne Cd, Cu, Pb, Ni, and Zn to first-instar Chironomus riparius larvae. Arch Environ Contam Toxicol 54:454–459. https://doi.org/10.1007/s00244-007-9048-7
Behmer ST (2008) Nutrition in insects. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Cham, pp 2646–2654. https://doi.org/10.1007/978-1-4020-6359-6_2277
Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82(8):493–512. https://doi.org/10.1007/s00204-008-0313-y
Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6(9):e04691. https://doi.org/10.1016/j.heliyon.2020.e04691
Cannino G, Ferruggia E, Luparello C, Rinaldi AM (2009) Cadmium and mitochondria. Mitochondrion 9(6):377–384. https://doi.org/10.1016/j.mito.2009.08.009
Chandran R, Sivakumar AA, Mohandass S, Aruchami M (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina Fulica. Comp Biochem Phys C 140(3–4):422–426. https://doi.org/10.1016/j.cca.2005.04.007
Cohen AC (2015) Insect diets: science and technology. CRC Press, Boca Raton
Dar MI, Green ID, Naikoo MI, Khan FA, Ansari AA, Lone MI (2017) Assessment of biotransfer and bioaccumulation of cadmium, lead and zinc from fly ash amended soil in mustard–aphid–beetle food chain. Sci Total Environ 584:1221–1229. https://doi.org/10.1016/j.scitotenv.2017.01.186
Deckert J (2005) Cadmium toxicity in plants: is there any analogy to its carcinogenic effect in mammalian cells? Biometals 18(5):475–481. https://doi.org/10.1007/s10534-005-1245-0
Długaszek M (2019) Studies on relationships between essential and toxic elements in selected body fluids, cells and tissues. Chem-Biol Interact 297:57–66. https://doi.org/10.1016/j.cbi.2018.10.011
Dow JA (2017) The essential roles of metal ions in insect homeostasis and physiology. Curr Opin Insect Sci 23:43–50. https://doi.org/10.1016/j.cois.2017.07.001
Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Environ Res Public Health 17(11):3782. https://doi.org/10.3390/ijerph17113782
Gintenreiter 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 Con Tox 25(1): 55–61. https://doi.org/10.1007/BF00230711
Grubor-Lajsic G, Block W, Palanacki V, Glumac S (1991) Cold hardiness parameters of overwintering diapause larvae of Ostrinia nubilalis in Vojvodina, Yugoslavia. Cryo-Letters 12:177–182
Grubor-Lajsic G, Block W, Worland R (1992) Comparison of the cold hardiness of two larval Lepidoptera (Noctuidae). Physiol Entomol 17(2):148–152. https://doi.org/10.1111/j.1365-3032.1992.tb01192.x
Himeno S, Yanagiya T, Fujishiro H (2009) The role of zinc transporters in cadmium and manganese transport in mammalian cells. Biochimie 91(10):1218–1222. https://doi.org/10.1016/j.biochi.2009.04.002
ISO/IEC 17025 (2017) General requirements for the competence of testing and calibration laboratories. International Organization for Standardization, Genève, Switzerland.
Jakimska A, Konieczka P, Skóra K, Namieśnik J (2011) Bioaccumulation of metals in tissues of marine animals, part i: the role and impact of heavy metals on organisms. Pol J Environ Stud 20(5):1117–1125
Kang YJ (2006) Metallothionein redox cycle and function. Exp Biol Med (maywood) 231(9):1459–1467. https://doi.org/10.1177/153537020623100903
Kojić D, Popović ŽD, Orčić D, Purać J, Orčić S, Vukašinović EL, Nikolić TV, Blagojević DP (2018) The influence of low temperature and diapause phase on sugar and polyol content in the European corn borer Ostrinia nubilalis (Hbn.). J Insect Physiol 109:107–113. https://doi.org/10.1016/j.jinsphys.2018.07.007
Krężel A, Maret W (2017) The functions of metamorphic metallothioneins in zinc and copper metabolism. Int J Mol Sci 18(6):1237. https://doi.org/10.3390/ijms18061237
Lewis LC (1975) Natural regulation of crop pests in their indigenous ecosystems and in Iowa agroecosystems: bioregulation of economic insect pests. Iowa State J Res 49:435–445
Lindqvist L, Block M (1995) Excretion of cadmium during moulting and metamorphosis in Tenebrio molitor (Coleoptera; Tenebrionidae). Comp Biochem Phys C 111(2):325–328. https://doi.org/10.1016/0742-8413(95)00057-U
Markert B, Fränzle S, Wünschmann S (2015) Chemical evolution: the biological system of the elements. Springer, Cham. https://doi.org/10.1007/978-3-319-14355-2_2
Martelli A, Rousselet E, Dycke C, Bouron A, Moulis JM (2006) Cadmium toxicity in animal cells by interference with essential metals. Biochimie 88(11):1807–1814. https://doi.org/10.1016/j.biochi.2006.05.013
Matović V, Buha A, Bulat Z, Đukić-Ćosić D (2011) Cadmium toxicity revisited: focus on oxidative stress induction and interactions with zinc and magnesium. Arh Hig Rada Toksiko 62(1):65–75. https://doi.org/10.2478/10004-1254-62-2011-2075
Merritt TJS, Bewick AJ (2017) Genetic diversity in insect metal tolerance. Front Genet 8:172. https://doi.org/10.3389/fgene.2017.00172
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. Biologia-Bratislava 59(5):645–654
Mohr SE, Killilea DW (2018) Metal biology takes flight: the study of metal homeostasis and detoxification in insects. Front Genet 9:221. https://doi.org/10.3389/fgene.2018.00221
Moulis JM (2010) Cellular mechanisms of cadmium toxicity related to the homeostasis of essential metals. Biometals 23(5):877–896. https://doi.org/10.1007/s10534-010-9336-y
Oonincx DGAB, Finke MD (2021) Nutritional value of insects and ways to manipulate their composition. J Insects Food Feed 7(5):639–659. https://doi.org/10.3920/JIFF2020.0050
Ortel J (1995) Accumulation of Cd and Pb in successive stages of Galleria mellonella and metal transfer to the pupal parasitoid Pimpla turionellae. Entomol Exp Appl 77(1):89–97. https://doi.org/10.1111/j.1570-7458.1995.tb01989.x
Ponsard S, Bethenod MT, Bontemps A, Pélozuelo L, Souqual MC, Bourguet D (2004) Carbon stable isotopes: a tool for studying the mating, oviposition, and spatial distribution of races of European corn borer, Ostrinia nubilalis, among host plants in the field. Can J Zool 82(7):1177–1185. https://doi.org/10.1139/z04-075
Popović ŽD, Subotić A, Nikolić TV, Radojičić R, Blagojević DP, Grubor-Lajšić G, Koštál V (2015) Expression of stress-related genes in diapause of European corn borer (Ostrinia nubilalis Hbn.). Comp Biochem Physiol B 186:1–7. https://doi.org/10.1016/j.cbpb.2015.04.004
Poteat MD, Díaz-Jaramillo M, Buchwalter DB (2012) Divalent metal (Ca, Cd, Mn, Zn) uptake and interactions in the aquatic insect Hydropsyche sparna. J Exp Biol 215(9):1575–1583. https://doi.org/10.1242/jeb.063412
Purać J, Nikolić TV, Kojić D, Ćelić AS, Plavša JJ, Blagojević DP, Petri ET (2019) Identification of a metallothionein gene in honey bee Apis mellifera and its expression profile in response to Cd. Cu and Pb Exposure Mol Ecol 28(4):731–745. https://doi.org/10.1111/mec.14984
Purać J, Čelić TV, Vukašinović EL, Đorđievski S, Milić S, Ninkov J, Kojić D (2021) Identification of a metallothionein gene and the role of biological thiols in stress induced by short-term Cd exposure in Ostrinia nubilalis. Comp Biochem Phys C 250:109148. https://doi.org/10.1016/j.cbpc.2021.109148
Rubino FM (2015) Toxicity of Glutathione-binding metals: a review of targets and mechanisms. Toxics 3(1):20–62. https://doi.org/10.3390/toxics3010020
Sandbichler AM, Höckner M (2016) Cadmium protection strategies-a hidden trade-off? Int J Mol Sci 17(1):139. https://doi.org/10.3390/ijms17010139
Stegeman JJ, Brouwer M, Di Giulio RT, Forlin L, Fowler BA, Sanders BM, VanVeld PA (1992) Enzyme and protein synthesis as indicator of contaminant exposure and effect. In: Huggett RJ, Kimmerle RA, Mehrle PM, Bergman HL (eds) Biomarkers: biochemical, physiological and histological markers of anthropogenic stress. SETAC Special Publication Series, Lewis Publisher, Chelsea, pp 235–335
Tamás MJ, Fauvet B, Christen P, Goloubinoff P (2018) Misfolding and aggregation of nascent proteins: a novel mode of toxic cadmium action in vivo. Curr Genet 64(1):177–181. https://doi.org/10.1007/s00294-017-0748-x
Thévenod F, Wolff NA (2016) Iron transport in the kidney: implications for physiology and cadmium nephrotoxicity. Metallomics 8(1):17–42. https://doi.org/10.1039/c5mt00215j (PMID: 26485516)
US EPA 2001 Method 200.7: Trace elements in water, solids, and biosolids by inductively coupled plasma—atomic emission spectrometry, Rev. 5 EPA-821-R-01- 010 2001.
Uzelac I, Avramov M, Čelić T, Vukašinović E, Gošić-Dondo S, Purać J, Kojić D, Blagojević D, Popović ŽD (2020) Effect of cold acclimation on selected metabolic enzymes during diapause in The European Corn Borer Ostrinia nubilalis (Hbn.). Sci Rep 10: 9085. https://doi.org/10.1038/s41598-020-65926-w
van Straalen NM, Roelofs D (2005) Cadmium tolerance in a soil arthropod. A model of real-time microevolution. Entomol Ber 65(4): 105–111.
Vlahović M, Matić D, Mutić J, Trifković J, Đurđić S, Mataruga VP (2017) Influence of dietary cadmium exposure on fitness traits and its accumulation (with an overview on trace elements) in Lymantria dispar larvae. Comp Biochem Phys C 200:27–33. https://doi.org/10.1016/j.cbpc.2017.06.003
Vukašinović EL, Pond DW, Grubor-Lajšić G, Worland MR, Kojić D, Purać J, Popović ZD, Blagojević DP (2018) Temperature adaptation of lipids in diapausing Ostrinia nubilalis: an experimental study to distinguish environmental versus endogenous controls. J Comp Physiol B Biochem Syst Environ Physiol 188:27–36. https://doi.org/10.1007/s00360-017-1110-9
Vukašinović EL, Čelić TV, Kojić D, Franeta F, Milić S, Ninkov J, Blagojević D, Purać J (2020) The effect of long term exposure to cadmium on Ostrinia nubilalis growth, development, survival rate and oxidative status. Chemosphere 243:125375. https://doi.org/10.1016/j.chemosphere.2019.125375
Wang J, Zhang P, Shen Q, Wang Q, Liu D, Li J, Wang L (2013) The effects of Cd exposure on the oxidative state and cell death in the gill of fresh water crab Sinapotamon henanense. PLoS ONE 8:e64020. https://doi.org/10.1371/journal.pone.0064020
Wenzl T, Haedrich J, Schaechtele A, Piotr R, Stroka J, Eppe G, Scholl G (2016) Guidance document on the estimation of LOD and LOQ for measurements in the field of contaminants in feed and food. EUR 28099. Publications Office of the European Union, Luxembourg, ISBN 978–92–79–61768–3. https://doi.org/10.2787/8931
Zachariassen KE, Kristiansen E, Pedersen SA (2004) Inorganic ions in cold-hardiness. Cryobiology 48(2):126–133. https://doi.org/10.1016/j.cryobiol.2004.01.004
Acknowledgements
Authors are thankful to Dr. Filip Franeta for providing biological material (O. nubilalis egg masses from the corn field), as well as for valuable and constructive suggestions during the planning and development of this research work.
Funding
The authors acknowledge financial support of the Ministry of Education, Science and Technological Development of the Republic of Serbia [Grant No. 451-03-68/2022–14/200125].
Author information
Authors and Affiliations
Contributions
JP, ELV and TVC designed the study. Material preparation and analysis were performed by DK, SO, SM and JV. ELV and TVC statistically analyzed data. The first draft of the manuscript was written by TVC and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Čelić, T.V., Vukašinović, E.L., Kojić, D. et al. Exposure to High Concentrations of Cadmium Which Delay Development of Ostrinia Nubilalis Hbn. Larvae Affected the Balance of Bioelements. Arch Environ Contam Toxicol 83, 193–200 (2022). https://doi.org/10.1007/s00244-022-00953-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-022-00953-4