Eco-friendly postharvest irradiation strategy with ¹³¹I isotope for environmental management of populations of migratory locust, Locusta migratoria

Abstract

Purpose

Irradiation of food is promising for control of pests to minimize postharvest losses of yields and thus improvement of food safety, shelf life of produce. It is a method of choice that induces a series of lethal biochemical and molecular changes culminating into the engagement of a downstream cascade to cause abnormalities in irradiated pests. In this study, the effects of iodine-131 (¹³¹I) isotope radiation on the male gonad development of the migratory locust, Locusta migratoria, were evaluated.

Materials and methods

Newly emerged adult male locusts, less than one-day-old, were divided into two groups, control and irradiated. Locusts in the control group (n = 20 insects) didn’t drink irradiated water and were reared under normal environmental conditions for one week. Locusts in the irradiated group (n = 20 insects) were exposed to irradiated water at a dose of 30 mCi and they were subsequently observed until they drank the whole quantity.

Results

At the end of the experiment, scanning and electron microscopic examination of testes obtained from irradiated locusts revealed several major abnormalities, including malformed nuclei of spermatozoa, irregular plasma membranes, shrinkage of testicular follicles, vacuolated cytoplasm, disintegrated nebenkern and agglutinations of spermatids. Flow cytometry analysis revealed that ¹³¹I radiation induced both early and late apoptosis, but not necrosis, in testicular tissues. Testes of irradiated insects also exhibited a burst in reactive oxygen species (ROS), as indicated by significant elevation in amounts of malondialdehyde (MDA), a marker for peroxidation of lipids. In contrast, irradiation coincided with significant reductions in activities of enzymatic antioxidant biomarkers. Relative to controls, a three-fold upregulation of expression of mRNA of heat shock protein, Hsp90, was observed in testicular tissue of irradiated locusts. ¹³¹I-irradiated insects exhibited genotoxicity, as indicated by significant increases in various indicators of DNA damage by the comet assay, including tail length (7.80 ± 0.80 µm; p < .01), olive tail moment (40.37 ± 8.08; p < .01) and tail DNA intensity % (5.1 ± 0.51; p < .01), in testicular cells compared to the controls.

Conclusion

This is the first report on elucidation of I¹³¹-irradiation-mediated histopathological, biochemical and molecular mechanisms in gonads of male L. migratoria. Herein, the findings underscore the utility of ¹³¹I radiation as an eco-friendly postharvest strategy for management of insect pests and in particular for control of populations of L. migratoria.

Graphical Abstract

Keywords:

• Pest control
• reproduction
• radiation
• annexin V-FITC
• Hsp90

Acknowledgements

Prof. Giesy was supported by the Canada Research Chair program, a Distinguished Visiting Professorship in the Department of Environmental Sciences, Baylor University in Waco, TX, USA.

Ethical approval

This article does not contain any studies with human participants, and studies with insects do not require an approval from ethics committee.

Author contributions

L.M.E and A.E.W. designed the study. N.A.T., M.M., N.K., and A.M.E. conducted the practical experiments. N.A.T. and M.M. drafted the manuscript and prepared the first version of figures. J.P.G. edited the article. A.E.W. re-organized the figures, wrote, reviewed and edited the manuscript. All authors read and approved the final version of the article.

Consent form

Not applicable.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

All data generated and analyzed in this study are included in this article.

Additional information

Funding

No funds was received for conducting this study.

Notes on contributors

Noura A. Toto

Noura A. Toto is currently a lecturer of entomology in the Department of Zoology at the Faculty of Science at Damanhur University, Egypt. Her research interests address topics in biological control of insects, insect physiology, forensic entomology, and nanotechnology research in insects.

Marian Malak

Marian Malak is an entomology lecturer in the Biological and Geological Sciences Department, Faculty of Education, Alexandria University, and practices insect molecular biology. Her research interests include the control, physiology, biochemistry, and chemical ecology of insects.

Nessrin Kheirallah

Nessrin Kheirallah is working as an associate professor in the Zoology Department, Faculty of Science, Alexandria University. She has wide experience in the area of animal ecology and its related disciplines. She has published many scientific papers focusing on pollutants and their related impacts on the environment.

Ahmed M. Eldrieny

Ahmed M. ElDrieny is currently a bio-physics lecturer at Radiology and Medical Imaging Technology Department, Pharos University. He got his radiation protection officer license and became interested in radiation biology, radioactive waste, and nanotechnology research. Moreover, he is a senior medical physicist and Head of Department of Medical Physics at Borg El Arab Alexandria University Hospital which encouraged him to be implicated within research in the field of fighting cancer.

Lamia M. El-Samad

Lamia M. El-Samad is currently a professor of environmental entomology at the Faculty of Science, Alexandria University, Egypt. She published several research papers and participated in international projects collaboration. Her main research interests include insect cell biology, insect physiology, ecology and biological control.

John P. Giesy

Professor John P. Giesy is a world leading eco-toxicologist and environmental chemist. He is also the recipient of many national and international awards. He has published 1385 peer-reviewed works and is the most cited author in Ecology and Environmental Sciences, with an H index of 137. His i10 Index is 1021 publications.

Abeer El Wakil

Abeer El Wakil is a professor of molecular biology based at the Faculty of Education, Alexandria University, Egypt. Her research focuses on cancer biology and microenvironment as well as biological and mechanistic studies of natural products. She has had a wide range of leadership experience in the fields of education, scientific research, and international relations at the hands of many distinguished scholars in Egypt and in prestigious European universities and research centers in France, Sweden, Germany, and the Netherlands.