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Journal of Integrative Agriculture  2024, Vol. 23 Issue (1): 195-204    DOI: 10.1016/j.jia.2023.08.010
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Tissue distribution of cadmium and its effect on reproduction in Spodoptera exigua

Honghua Su1, Menglu Wu1, Yong Yang1, Yan Deng1, Yizhong Yang1#, Qingming Sun2#

1 College of Plant Protection, Yangzhou University, Yangzhou 225009, China

2 Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences/Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture and Rural Affairs/Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou 510640, China

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摘要  

蔬菜田极易受到重金属污染。甜菜夜蛾是主要的蔬菜害虫,主要通过取食受到重金属的胁迫。本文研究了镉胁迫下甜菜夜蛾不同组织中镉的积累及其对母代和子代生长发育的影响。在不同浓度(0.23.251.2 mg kg-1)镉的胁迫下,甜菜夜蛾各组织中镉含量与饲料中镉浓度相关。在幼虫阶段,三种镉处理中,中肠镉累积量最高,但成虫阶段,脂肪体中的镉含量最高;此外,卵巢中镉的含量显著高于精巢。甜菜夜蛾F1代分别取食不同浓度含镉饲料,而F2代均取食不含镉的人工饲料,在51.2 mg kg-1镉处理下,甜菜夜蛾F2代的幼虫存活率、化蛹率、羽化率和繁殖力较F1代均显著下降;3.2 mg kg-1处理后的F2代的繁殖力也明显低于亲代。在3.251.2 mg kg-1的镉胁迫下,仅雌虫受胁迫的繁殖力显著低于仅雄虫受胁迫的处理;母代在幼虫期受51.2 mg kg-1镉胁迫后,F2代的繁殖力显著低于F1代,同时显著低于3.20.2 mg kg-1处理下的繁殖力。该研究可作为不同重金属胁迫下的种群增长趋势预测的依据,也可为重金属污染环境风险评价提供有效参考。



Abstract  

Vegetable fields are often contaminated by heavy metals, and Spodoptera exigua is a major vegetable pest which is stressed by heavy metals mainly by feeding.  In this study, cadmium accumulation in the tissues of Sexigua exposed to cadmium and its effects on the growth and development of the parents and the offspring were investigated.  Under the stress of different concentrations of cadmium (0.2, 3.2, and 51.2 mg kg–1), the cadmium content in each tissue of Sexigua increased in a dose-dependent manner.  At the larval stage, the highest cadmium accumulation was found in midgut in all three cadmium treatments, but at the adult stage, the highest cadmium content was found in fat body.  In addition, the cadmium content in ovaries was much higher than in testes.  When F1 Sexigua was stressed by cadmium and the F2 generation was not fed a cadmium-containing diet, the larval survival, pupation rate, emergence rate and fecundity of the F2 generation were significantly reduced in the 51.2 mg kg–1 treatment compared to the corresponding F1 generation.  Even in the F2 generation of the 3.2 mg kg–1 treatment, the fecundity was significantly lower than in the parental generation.  The fecundity of the only-female stressed treatment was significantly lower than that of the only-male stressed treatment at the 3.2 and 51.2 mg kg–1 cadmium exposure levels.  When only mothers were stressed at the larval stage, the fecundity of the F2 generation was significantly lower than that of the F1 generation in the 51.2 mg kg–1 treatment, and it was also significantly lower than in the 3.2 and 0.2 mg kg–1 treatments.  The results of our study can provide useful information for forecasting the population increase trends under different heavy metal stress conditions and for the reliable environmental risk assessment of heavy metal pollution.


Keywords:  heavy metal pollution        cadmium, Spodoptera exigua        tissue distribution        reproduction   
Received: 16 February 2023   Accepted: 12 July 2023
Fund: This study was partially supported by the Open Project Program from the Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization (Ministry of Agriculture and Rural Affairs), China (212103).
About author:  Honghua Su, E-mail: susugj@126.com; #Correspondence Yizhong Yang, Tel: +86-514-87979344, E-mail: yzyang@yzu.edu.cn; Qingming Sun, Tel: +86-20-38765390, E-mail: qingmingsun@126.com

Cite this article: 

Honghua Su, Menglu Wu, Yong Yang, Yan Deng, Yizhong Yang, Qingming Sun. 2024. Tissue distribution of cadmium and its effect on reproduction in Spodoptera exigua. Journal of Integrative Agriculture, 23(1): 195-204.

Ashraf I, Ahmad F, Sharif A, Altaf A R, Teng H. 2021. Heavy metals assessment in water, soil, vegetables and their associated health risks via consumption of vegetables, District Kasur, Pakistan. SN Applied Sciences, 3, 552.

Augustyniak M, Plachetka-Bozek A, Kafel A, Babczynska A, Tarnawska M, Janiak A, Loba A, Dziewiecka M, Karpeta-Kaczmarek J, Zawisza-Raszka A. 2016. Phenotypic plasticity, epigenetic or genetic modifications in relation to the duration of Cd-exposure within a microevolution time range in the beet armyworm. PLoS ONE, 11, e0167371.

Augustyniak M, Tarnawska M, Babczynska A, Kafel A, Zawisza-Raszka A, Adamek B, Plachetka-Bozek A. 2017. Cross tolerance in beet armyworm: Long-term selection by cadmium broadens tolerance to other stressors. Ecotoxicology, 26, 1408–1418.

Ballan-Dufrancaiss C. 2002. Localization of metals in cells of pterygote insects. Microscopy Research and Technique, 56, 403–420.

Bebas P, Kotwica J, Joachimiak E, Giebultowicz J M. 2008. Yolk protein is expressed in the insect testis and interacts with sperm. BMC Developmental Biology, 8, 64.

Cervera A, Cristina M A, Martinez-Pardo R, Dolores G M. 2005. Vitellogenesis inhibition in Oncopeltus fasciatus females (Heteroptera: Lygaeidae) exposed to cadmium. Journal of Insect Physiology, 51, 895–911.

Cervera A, Maymó A C, Sendra M. 2004. Cadmium effects on development and reproduction of Oncopeltus fasciatus (Heteroptera: Lygaeidae). Journal of Insect Physiology, 50, 737–749.

Crawford L A, Lepp N W, Hodkinson I D. 1996. Accumulation and egestion of dietary copper and cadmium by the grasshopper Locusta migratoria R & F (Orthoptera: Acrididae). Environmental Pollution, 92, 241–246.

Devkota B, Schmidt G H. 2000. Accumulation of heavy metals in food plants and grasshoppers from the Taigetos Mountains Greece. Agriculture, Ecosystems and Environment, 78, 85–91.

Engelmann F. 1979. Insect vitellogenin: Identification, biosynthesis, and role in vitellogenesis. Advances in Insect Physiology, 14, 49–108.

Gall J E, Boyd R S, Rajakaruna N. 2015. Transfer of heavy metals through terrestrial food webs: A review. Environmental Monitoring and Assessment, 187, 201.

Gintenreiter S, Ortel J, Nopp H J. 1993. Effects of different dietary levels of cadmium, lead, copper, and zinc on the vitality of the forest pest insect Lymantria dispar L. (Lymantriidae, Lepid). Archives of Environmental Contamination and Toxicology, 25, 62–66.

Hu M M, Cai W C, Su H H, Yang Y Z. 2014. Accumulation of lead in Spodoptera exigua (Hübner) and its impact on the population. Chinese Journal of Applied Ecology, 25, 1145–1150. (in Chinese)

Hunter B A, Hunter L M, Johnson M S. 1987. Dynamics of metal accumulation in the grasshopper Chorthippus brunneus in contaminated grasslands. Archives of Environmental Contamination and Toxicology, 16, 711–716.

Jiang D, Tan M, Guo Q, Yan S. 2020. Transfer of heavy metal along food chain: A mini-review on insect susceptibility to entomopathogenic microorganisms under heavy metal stress. Pest Management Science, 77, 1115–1120.

Kafel A, Nowak A, Bembenek J, Szczygiel J, Nakonieczny M, Swiergosz-Kowalewska R. 2012a. The ocalization of HSP70 and oxidative stress indices in heads of Spodoptera exigua larvae in a cadmium-exposed population. Ecotoxicology and Environmental Safety, 78, 22–27.

Kafel A, Rozpedek K, Szulinska E, Zawisza-Raszka A, Migula P. 2014. The effects of cadmium or zinc multigenerational exposure on metal tolerance of Spodoptera exigua (Lepidoptera: Noctuidae). Environmental Science and Pollution Research, 21, 4705–4715.

Kafel A, Zawisza-Raszka A, Szulinska E. 2012b. Effects of multigenerational cadmium exposure of insects (Spodoptera exigua larvae) on anti-oxidant response in haemolymph and developmental parameters. Environmental Pollution, 162, 8–14.

Krams I, Kecko S, Kangassalo K, Moore F R, Jankevics E, Inashkina I, Krama T, Lietuvietis V, Meija L, Rantala M J. 2015. Effects of food quality on trade-offs among growth, immunity and survival in the greater wax moth Galleria mellonella. Insect Science, 22, 431–439.

Kubota R, Kunito T, Tanabe S, Ogi H, Shibata Y. 2002. Maternal transfer of arsenic to eggs of black-tailed gull (Larus crassirostris) from Rishiri Island, Japan. Applied Organometallic Chemistry, 16, 463–468.

Li K, Chen J, Jin P, Li J, Wang J, Shu Y. 2018. Effects of Cd accumulation on cutworm Spodoptera litura larvae via Cd treated Chinese flowering cabbage Brassica campestris and artificial diets. Chemosphere, 200, 151–163.

Luo M, Cao H M, Fan Y Y, Zhou X C, Chen J X, Chung H, Wei H Y. 2019. Bioaccumulation of cadmium affects development, mating behavior, and fecundity in the Asian Corn Borer, Ostrinia furnacalis. Insects, 11, 7.

MEP (Ministry of Environmental Protection of China). 2014. National Soil Pollution Survey Bulletin. [2019-5-6]. https://www.mee.gov.cn/gkml/sthjbgw/qt/201404/t20140417_270670.htm (in Chinese)

Mese Y, Tuncsoy B, Ozalp P. 2022. Effects of Cu, Zn and their mixtures on bioaccumulation and antioxidant enzyme activities in Galleria mellonella L. (Lepidoptera: Pyralidae). Ecotoxicology, 31, 649–656.

Mikkola K, Rantala M J. 2010. Immune defence, a possible nonvisual selective factor behind the industrial melanism of moths (Lepidoptera). Biological Journal of the Linnean Society, 99, 831–838.

Monsefi M, Alaee S, Moradshahi A, Rohani L. 2010. Cadmium-induced infertility in male mice. Environmental Toxicology, 25, 94–102.

Nishizono H, Ichikawa H, Suziki S, Ishii F. 1987. The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant and Soil, 101, 15–20.

Niu C Y. 2000. Responses of housefly (Muscadomestica) to heavy metals and studies of the related metallothionein. Ph D thesis, Institute of Applied Entomology, Zhejiang University, China. (in Chinese)

Pang J, Lu R G, Qiu Q W. 2011. Simultaneous determination of arsenic and mercury in drinking water by hydride-gener-ation atomic fluorescence spectrometry. Chinese Journal of Health Laboratory Technology, 21, 1898–1899, 1902. (in Chinese)

Plachetka-Bozek A, Chwialkowska K, Augustyniak M. 2018a. Molecular changes in vitellogenin gene of Spodoptera exigua after long-time exposure to cadmium - Toxic side effect or microevolution? Ecotoxicology and Environmental Safety, 147, 461–470.

Plachetka-Bozek A, Kafel A, Augustyniak M. 2018b. Reproduction and development of Spodoptera exigua from cadmium and control strains under differentiated cadmium stress. Ecotoxicology and Environmental Safety, 166, 138–145.

Smigiel D. 1994. Accumulation of heavy metals (Pb, Cd) in selected varieties of vegetables. Roczniki Panstwowego Zakladu Higieny, 45, 279–284.

Su H H, Wu J J, Zhang Z X, Ye Z B, Chen Y Q, Yang Y Z. 2021. Effects of cadmium stress at different concentrations on the reproductive behaviors of beet armyworm Spodoptera exigua (Hübner). Ecotoxicology, 30, 402–410.

Sun H X, Xia Q, Zhou Q, Zhang G R. 2008. Accumulation and excretion of nickel in Spodoptera litura Fabricius larvae fed on diets with Ni2+. Acta Entomologica Sinica, 51, 569–574.

Suzuki K T, Aoki Y, Nishikawa M, Masui H, Matsubara F. 1984. Effect of cadmium-feeding on tissue concentration of elements in germ-free silkworm (Bombyx mori) larvae and distribution in the alimentary canal. Comparative Biochemistry and Physiology, 79, 249–253.

Thompson J, Bannigan J. 2008. Cadmium: Toxic effects on the reproductive system and the embryo. Reproductive Toxicology, 25, 304–315.

Wilczek G, Babczynska A, Augustyniak M, Migula P. 20004. Relations between metals (Zn, Pb, Cd and Cu) and glutathione-dependent detoxifying enzymes in spiders from a heavy metal pollution gradient. Environmental Pollution, 132, 453–461.

Wu G X, Zhu J Y, Gao X, Ye G Y, Hu C, Cheng J A. 2010. Study on accumulation and excretion of dietary cadmium and copper by Boettcherisca peregrine (Diptera: Sarcophagidae). Journal of Environmental Entomology, 32, 347–352. (in Chinese)

Yang Q Q, Li Z Y, Lu X N, Duan Q N, Huang L, Bi Jun. 2018. A review of soil heavy metal pollution from industrial and agricultural regions in China: Pollution and risk assessment. Science of The Total Environment, 642, 690–700.

Yu X H. 2008. Effects of cadmium on the performance of Oryza satrva L. and Nilaparvata lugens Stål. MSc thesis, Fujian Agriculture and Forestry University, China. (in Chinese)

Zhou J, Shu Y, Zhang G, Zhou Q. 2012a. Lead exposure improves the tolerance of Spodoptera litura (Lepidoptera: Noctuidae) to cypermethrin. Chemosphere, 88, 507–513.

Zhou J, Zhang G, Zhou Q. 2012b. Molecular characterization of cytochrome P450 CYP6B47 cDNAs and 5’-flanking sequence from Spodoptera litura (Lepidoptera: Noctuidae): Its response to lead stress. Journal of Insect Physiology, 58, 726–736.

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