Impact of clothianidin exposure on the growth, metabolism, and neurological function of Penaeus vannamei
Zhi Luo , Zhen-Fei Li , Zhi-Yu Lin , Zhen-Qiang Fu , Feng-Lu Han , Er-Chao Li
Stress Biology ›› 2025, Vol. 5 ›› Issue (1) : 67
Impact of clothianidin exposure on the growth, metabolism, and neurological function of Penaeus vannamei
Clothianidin, a widely used neonicotinoid pesticide, poses potential ecological risks to aquatic ecosystems due to its unique mode of action and widespread environmental dispersal. This study investigates the toxic effects of clothianidin on Penaeus vannamei at different concentrations over 28 days. High concentrations of clothianidin significantly affected shrimp physiology, as evidenced by changes in survival rate and weight gain. Markers of oxidative stress, including decreased respiratory burst, reduced glutathione levels, and diminished antioxidant enzyme activities, indicated that clothianidin triggered oxidative stress responses in shrimp. Additionally, changes in lactate dehydrogenase, succinate dehydrogenase, and isocitrate dehydrogenase activities suggested disruptions in energy metabolism in the hepatopancreas. Analysis of the nervous system revealed significant disturbances in neural signaling, reflected by altered levels of acetylcholine, acetylcholinesterase, and dopamine. Transcriptomic analysis highlighted significant changes in gene expression and metabolic processes in the nervous system. This study demonstrates that clothianidin disrupts oxidative balance, energy metabolism, and neural signaling, affecting the growth of P. vannamei and providing valuable insights into its biochemical and transcriptomic toxicity in aquatic environments.
Neonicotinoid insecticides / Toxicity / Shrimp / Mechanism
| [1] |
Ahmad MF, Ahmad FA, Alsayegh AA, Zeyaullah M, AlShahrani AM, Muzammil K, Saati AA, Wahab S, Elbendary EY, Kambal N, Abdelrahman MH, Hussain S (2024) Pesticides impacts on human health and the environment with their mechanisms of action and possible countermeasures. Heliyon 10:e29128. https://doi.org/10.1016/j.heliyon.2024.e29128 |
| [2] |
Anadón A, Ares I, Martínez M, Martínez-Larrañaga MR, Martínez MA (2020) Neurotoxicity of neonicotinoids. In: Aschner M, Costa LG (eds) Advances in neurotoxicology. Academic Press. https://doi.org/10.1016/bs.ant.2019.11.005 |
| [3] |
Anderson JC, Dubetz C, Palace VP (2015) Neonicotinoids in the Canadian aquatic environment: A literature review on current use products with a focus on fate, exposure, and biological effects. Sci Total Environ 505:409–422. https://doi.org/10.1016/j.scitotenv.2014.09.090 |
| [4] |
|
| [5] |
Bal R, Türk G, Tuzcu M, Yılmaz Ö, Kuloğlu T, Baydaş G, Naziroğlu M, Yener Z, Etem E, Tuzcu Z (2013) Effects of the neonicotinoid insecticide, clothianidin, on the reproductive organ system in adult male rats. Drug Chem Toxicol 36:421–429. https://doi.org/10.3109/01480545.2013.776575 |
| [6] |
|
| [7] |
Bhutia YD, Ganapathy V (2018) Protein digestion and absorption. In: Johnson LR (eds) Physiology of the gastrointestinal tract. Elsevier Academic Press. https://doi.org/10.1016/B978-0-12-809954-4.00047-5 |
| [8] |
Borregaard N (1988) The respiratory burst: an overview. In: Sbarra AJ, Strauss RR (eds) The respiratory burst and its physiological significance. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5496-3_1 |
| [9] |
Butcherine P, Kelaher BP, Taylor MD, Lawson C, Benkendorff K (2021) Acute toxicity, accumulation and sublethal effects of four neonicotinoids on juvenile Black Tiger Shrimp (Penaeus monodon). Chemosphere 275:129918. https://doi.org/10.1016/j.chemosphere.2021.129918 |
| [10] |
Cech R, Zaller JG, Lyssimachou A, Clausing P, Hertoge K, Linhart C (2023) Pesticide drift mitigation measures appear to reduce contamination of non-agricultural areas, but hazards to humans and the environment remain. Sci Total Environ 854:158814. https://doi.org/10.1016/j.scitotenv.2022.158814 |
| [11] |
Copani A, Caraci F, Hoozemans JJ, Calafiore M, Sortino MA, Nicoletti F (2007) The nature of the cell cycle in neurons: focus on a "non-canonical" pathway of DNA replication causally related to death. Biochim Biophys Acta-Mol Basis Dis. 1772:409–412. https://doi.org/10.1016/j.bbadis.2006.10.016 |
| [12] |
Cori CF, Cori GT (1946) Carbohydrate metabolism. Annu Rev Biochem 15:193–218. https://doi.org/10.1101/cshperspect.a040568 |
| [13] |
|
| [14] |
|
| [15] |
Duggan PF (1977) An enzyme system requiring magnesium, calcium and potassium ions. Proc R Ir Acad B 77(19-47):449–455 |
| [16] |
|
| [17] |
|
| [18] |
Fu Z, Han F, Huang K, Zhang J, Qin JG, Chen L, Li E (2022a) Impact of imidacloprid exposure on the biochemical responses, transcriptome, gut microbiota and growth performance of the Pacific white shrimp Litopenaeus vannamei. J Hazard Mater 424:127513. https://doi.org/10.1016/j.jhazmat.2021.127513 |
| [19] |
Fu Z, Han F, Huang K, Zhang J, Qin JG, Chen L, Li E (2022b) Combined toxic effects of thiamethoxam on intestinal flora, transcriptome and physiology of Pacific white shrimp Litopenaeus vannamei. Sci Total Environ 830:154799. https://doi.org/10.1016/j.scitotenv.2022.154799 |
| [20] |
|
| [21] |
Hladik ML, Kolpin DW (2016) First national-scale reconnaissance of neonicotinoid insecticides in streams across the USA. Environ Chem 13:12–20. https://doi.org/10.1071/EN15061 |
| [22] |
|
| [23] |
|
| [24] |
|
| [25] |
|
| [26] |
Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:751. https://doi.org/10.3389/fpls.2018.00751 |
| [27] |
Le Corre V, Kremer A (2012) The genetic differentiation at quantitative trait loci under local adaptation. Mol Ecol 21:1548–1566. https://doi.org/10.1111/j.1365-294x.2012.05479.x |
| [28] |
|
| [29] |
Ling ZN, Jiang YF, Ru JN, Lu JH, Ding B, Wu J (2023) Amino acid metabolism in health and disease. Signal Transduct Target Ther 8:345. https://doi.org/10.1038/s41392-023-01569-3 |
| [30] |
Lowe R, Shirley N, Bleackley M, Dolan S, Shafee T (2017) Transcriptomics technologies. PLoS Comput Biol 13:e1005457. https://doi.org/10.1371/journal.pcbi.1005457 |
| [31] |
Luo Z, Lin ZY, Li ZF, Fu ZQ, Han FL, Li EC (2024) Next-generation neonicotinoid: The impact of cycloxaprid on the crustacean decapod Penaeus vannamei. Chemosphere 358:142150. https://doi.org/10.1016/j.chemosphere.2024.142150 |
| [32] |
Main AR, Headley JV, Peru KM, Michel NL, Cessna AJ, Morrissey CA (2014) Widespread Use and Frequent Detection of Neonicotinoid Insecticides in Wetlands of Canada's Prairie Pothole Region. PLoS ONE 9:e92821. https://doi.org/10.1371/journal.pone.0092821 |
| [33] |
|
| [34] |
Malhotra N, Chen KHC, Huang JC, Lai HT, Uapipatanakul B, Roldan MJM, Macabeo APG, Ger tr, Hsiao CD (2021) Physiological Effects of Neonicotinoid Insecticides on Non-Target Aquatic Animals—An Updated Review. Int J Mol Sci 22(17):9591. https://doi.org/10.3390/ijms22179591 |
| [35] |
Miles JC, Hua J, Sepulveda MS, Krupke CH, Hoverman JT (2017) Effects of clothianidin on aquatic communities: Evaluating the impacts of lethal and sublethal exposure to neonicotinoids. PLoS ONE 12:e0174171. https://doi.org/10.1371/journal.pone.0174171 |
| [36] |
|
| [37] |
|
| [38] |
Naidu BC, Xavier KAM, Sahana MD, Landge AT, Jaiswar AK, Shukla SP, Ranjeet K, Nayak BB (2025) Temporal variability of microplastics in shrimp (Litopenaeus vannamei), feed, water and sediments of coastal and inland culture ponds. Sci Total Environ 959:178173. https://doi.org/10.1016/j.scitotenv.2024.178173 |
| [39] |
Naiel MAE, Shehata AM, Negm SS, Abd El-Hack ME, Amer MS, Khafaga AF, Bin-Jumah M, Allam AA (2020) The new aspects of using some safe feed additives on alleviated imidacloprid toxicity in farmed fish: a review. Rev Aaquacult 12:2250–2267. https://doi.org/10.1111/raq.12432 |
| [40] |
Nersisyan S, Novosad V, Engibaryan N, Ushkaryov Y, Nikulin S, Tonevitsky A (2021) ECM–receptor regulatory network and its prognostic role in colorectal cancer. Front Genet 12:782699. https://doi.org/10.3389/fgene.2021.782699 |
| [41] |
|
| [42] |
|
| [43] |
Patil S, D'souza RC (2024) Effects of Clothianidin on Biochemical Parameters of Adult Zebrafish. J Adv Zool 45(3):406-417. http://doi.org/10.53555/jaz.v45i3.4304 |
| [44] |
|
| [45] |
|
| [46] |
Quinn DM (1987) Acetylcholinesterase: enzyme structure, reaction dynamics, and virtual transition states. Chem Rev 87:955–979. https://doi.org/10.1021/cr00081a005 |
| [47] |
|
| [48] |
|
| [49] |
|
| [50] |
|
| [51] |
Taylor SS, Yang J, Wu J, Haste NM, Radzio-Andzelm E, Anand G (2004) PKA: a portrait of protein kinase dynamics, Biochim Biophys Acta 1697:259–269. https://doi.org/10.1016/j.bbapap.2003.11.029 |
| [52] |
Terwilliger NB (2015) Oxygen transport proteins in Crustacea: hemocyanin and hemoglobin. In: Chang ES, Thiel M (eds) The Natural History of the Crustacea, Volume 4: Physiology. Oxford University Press, USA |
| [53] |
Tomoyasu Y, Miller SC, Tomita S, Schoppmeier M, Grossmann D, Bucher G (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol 9(1):R10. https://doi.org/10.1186/gb-2008-9-1-r10 |
| [54] |
|
| [55] |
|
| [56] |
Wang Y, Shen J, Li X, Lang H, Zhang L, Fang H, Yu Y (2023) Higher temperature and daily fluctuations aggravate clothianidin toxicity towards Limnodrilus hoffmeisteri. Sci Total Environ 903:166655. https://doi.org/10.1016/j.scitotenv.2023.166655 |
| [57] |
|
| [58] |
|
The Author(s)
/
| 〈 |
|
〉 |