Lead bioaccumulation in herbivorous insects and parasitoids reared on plants grown in lead-contaminated soil under field conditions

Authors

DOI:

https://doi.org/10.37486/2675-1305.ec06028

Keywords:

Aphids, Biomagnification, Heavy metals, Kale, Lepidopterans

Abstract

We investigated the lead (Pb) bioaccumulation in herbivorous insects and parasitoids on kale plants (Brassica oleracea var. acephala) cultivated in soils experimentally contaminated. We cultivated kale in soil with lead nitrate concentrations of 0 (control), 144, 360, and 600 mg/Kg of soil, representing permissible levels for Brazilian soils. The plants were kept in an open greenhouse to allow the natural colonization by insects under field conditions. We collected insects through direct removal or trap bags. Dried samples of leaves, herbivorous sap-sucking and chewing insects, and their respective parasitoids were analyzed utilizing ICP-OES to determine Pb concentrations. Pb was transferred in this system, with insects showing higher Pb content than leaves, and the highest values being found in parasitoids, which exhibited the highest levels ever recorded, even though our foliar Pb levels were lower than those in laboratory assays conducted up to then. These results indicate Pb biomagnification. We discuss Pb bioaccumulation effects on herbivores and parasitoids, comparing them with laboratory studies. We provide unprecedented insights into heavy metal bioaccumulation in field herbivorous insects and parasitoids.

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References

Ali, H.; Khan, E.; Ilahi, I. (2019a) Environmental Chemistry and Ecotoxicology of Hazardous Heavy Metals: Environmental Persistence, Toxicity, and Bioaccumulation. Journal of Chemistry, 2019: 6730305. doi: 10.1155/2019/6730305

Ali, S.; Ullah, M. I.; Saeed, M. F.; Khalid, S.; Saqib, M.; Arshad, M.; Afzal, M.; Damalas, C. A. (2019b) Heavy metal exposure through artificial diet reduces growth and survival of Spodoptera litura (Lepidoptera: Noctuidae). Environmental Science and Pollution Research, 26(14): 14426-14434. doi: 10.1007/s11356-019-04792-0

ANVISA (Agência Nacional de Vigilância Sanitária) (2021) Instrução Normativa - IN N° 88. Diário Oficial da União. https://www.in.gov.br/en/web/dou/-/instrucao-normativa-in-n-88-de-26-de-marco-de-2021-311655598

Chaffai, R.; Koyama, H. (2011) Heavy Metal Tolerance in Arabidopsis thaliana. Advances in Botanical Research, 60: 1-49. doi: 10.1016/B978-0-12-385851-1.00001-9

CODEX (Codex Alimentarius Commission) (2017) Joint FAO/WHO Food Standards Programme Codex Committee on Contaminants in Foods - Working Document for Information and Use in Discussions Related to Contaminants and Toxins in the GSCTFF. https://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FMeetings%252FCX-735-11%252FWD%252Fcf11_INF01x.pdf

Coleman, C. M.; Boyd, R. S.; Eubanks, M. D. (2005) Extending the Elemental Defense Hypothesis: Dietary Metal Concentrations Below Hyperaccumulator Levels Could Harm Herbivores. Journal of Chemical Ecology, 31(8): 1669-1681. doi: 10.1007/s10886-005-5919-4

CONAMA (Conselho Nacional do Meio Ambiente) (2013) Resolução nº 460. https://www.ibama.gov.br/component/legislacao/?view=legislacao&legislacao=131499

Dar, M. I.; Green, I. D.; Naikoo, M. I.; Khan, F. A.; Ansari, A. A.; Lone, M. I. (2017) Assessment of biotransfer and bioaccumulation of cadmium, lead and zinc from fly ash amended soil in mustard-aphid-beetle food chain. Science of the Total Environment, 584-585: 1221-1229. doi: 10.1016/j.scitotenv.2017.01.186

Edelstein, M.; Ben-Hur, M. (2018) Heavy metals and metalloids: Sources, risks and strategies to reduce their accumulation in horticultural crops. Scientia Horticulturae, 234: 431-444. doi: 10.1016/j.scienta.2017.12.039

Gintenreiter, S.; Ortel, J.; Nopp, H. J. (1993) Bioaccumulation of cadmium, lead, copper, and zinc in successive developmental stages of Lymantria dispar L. (Lymantriidae, Lepid) - a life cycle study. Archives of Environmental Contamination and Toxicology, 25(1): 55-61. doi: 10.1007/BF00230711

Jhee, E. M.; Boyd, R. S.; Eubanks, M. D. (2006) Effectiveness of Metal-Metal and Metal-Organic Compound Combinations Against Plutella xylostella: Implications for Plant Elemental Defense. Journal of Chemical Ecology, 32(2): 239-259. doi: 10.1007/s10886-005-9000-0

Kazimírová, M.; Ortel, J. (2000) Metal accumulation by Ceratitis capitata (Diptera) and transfer to the parasitic wasp Coptera occidentalis (Hymenoptera). Environmental Toxicology and Chemistry, 19(7): 1822-1829. h doi: 10.1002/etc.5620190716

Kazimirova, M.; Slovák, M.; Manova, A. (1997) Host parasitoid relationship of Ceratitis capitata (Diptera: Tephritidae) and Coptera occidentalis (Hymenoptera: Proctotrupoidea: Diapriidae) under host heavy metal stress. European Journal of Entomology, 94(3): 409-420.

Morales-Silva, T.; Silva, B. C.; Faria, L. D. B. (2022) Soil contamination with permissible levels of lead negatively affects the community of plant-associated insects: A case of study with kale. Environmental Pollution, 304: 119143. doi: 10.1016/j.envpol.2022.119143

Morales-Silva, T.; Silva, B. C., Silva; V. H. D.; Faria, L. D. B. (2023) Simplification effect of lead soil contamination on the structure and function of a food web of plant-associated insects. Agriculture, Ecosystems & Environment, 354: 108570. doi: 10.1016/j.agee.2023.108570

Naikoo, M. I.; Raghib, F.; Dar, M. I.; Khan, F. A.; Hessini, K.; Ahmad, P. (2021) Uptake, accumulation and elimination of cadmium in a soil - Faba bean (Vicia faba) - Aphid (Aphis fabae) - Ladybird (Coccinella transversalis) food chain. Chemosphere, 279: 130522. doi: 10.1016/j.chemosphere.2021.130522

Ortel, J. (1995) Accumulation of Cd and Pb in successive stages of Galleria mellonella and metal transfer to the pupal parasitoid Pimpla turionellae. Entomologia Experimentalis et Applicata, 77(1): 89-97. doi: 10.1111/j.1570-7458.1995.tb01989.x

Ortel, J.; Gintenreiter, S.; Nopp, H. (1993) The effects of host metal stress on a parasitoid in an insect/insect relationship (Lymantria dispar L., Lymantriidae, Lepid.-Glyptapanteles liparidis Bouchè, Braconidae, Hym.). Archives of Environmental Contamination and Toxicology, 24(4): 421-426. doi: 10.1007/BF01146156

R Core Team (2020) R: A language and environment for statistical computing. https://www.r-project.org.

Woźniak, A.; Bednarski, W.; Dancewicz, K.; Gabryś, B.; Borowiak-Sobkowiak, B.; Bocianowski, J.; Samardakiewicz, S.; Rucińska-Sobkowiak, R.; Morkunas, I. (2019) Oxidative stress links response to lead and Acyrthosiphon pisum in Pisum sativum L. Journal of Plant Physiology, 240: 152996. doi: 10.1016/j.jplph.2019.152996

Woźniak, A.; Drzewiecka, K.; Kęsy, J.; Marczak, Ł.; Narożna, D.; Grobela, M.; Motała, R.; Bocianowski, J.; Morkunas, I. (2017) The Influence of Lead on Generation of Signalling Molecules and Accumulation of Flavonoids in Pea Seedlings in Response to Pea Aphid Infestation. Molecules, 22(9): 1404. doi: 10.3390/molecules22091404

Wuana, R. A.; Okieimen, F. E. (2011) Heavy Metals in Contaminated Soils: A Review of Sources, Chemistry, Risks and Best Available Strategies for Remediation. ISRN Ecology, 2011: 1-20. doi: 10.5402/2011/402647

Ye, G. Y.; Dong, S. Z., Dong, H.; Hu, C.; Shen, Z. C.; Cheng, J. A. (2009) Effects of host (Boettcherisca peregrina) copper exposure on development, reproduction and vitellogenesis of the ectoparasitic wasp, Nasonia vitripennis. Insect Science, 16(1): 43-50. doi: 10.1111/j.1744-7917.2009.00252.x

Zhang, J.; Jiang, D.; Dong, X.; Meng, Z.; Yan, S. (2020) Accumulation of Cd and Pb in various body parts, organs and tissues of Lymantria dispar asiatica (Lepidoptera: Erebidae). Journal of Asia-Pacific Entomology, 23(4): 963-969. doi: 10.1016/j.aspen.2020.07.019

Zhou, J.; Shu, Y.; Zhang, G.; Zhou, Q. (2012) Lead exposure improves the tolerance of Spodoptera litura (Lepidoptera: Noctuidae) to cypermethrin. Chemosphere, 88(4): 507-513. doi: 10.1016/j.chemosphere.2012.03.011

Published

2024-11-07

How to Cite

Morales-Silva, T., Corrêa-Silva, B., & Faria, L. D. B. (2024). Lead bioaccumulation in herbivorous insects and parasitoids reared on plants grown in lead-contaminated soil under field conditions. Entomological Communications, 6, ec06028. https://doi.org/10.37486/2675-1305.ec06028

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