Effects of Single and Combined Exposure to Environmentally Relevant Concentrations of Cyfluthrin and Copper on Digestive Gland Histology of Lymnaea stagnalis

Year 2023, Volume 27, Issue 1, 39 - 48, 28.02.2023

Sezgi ARMAN

https://doi.org/10.16984/saufenbilder.1169843

Abstract

Pyrethroid insecticides and heavy metals frequently co-exist in aquatic systems, due to intensive anthropogenic activities, and their effects on aquatic organisms are needed to be investigated. In the present work, single and combined effects of environmentally realistic concentrations of cyfluthrin and copper on the digestive gland histology of the freshwater pond snail (Lymnaea stagnalis) were evaluated. Snails were exposed to 1 µg/L cyfluthrin, 10 µg/L copper, and 1 µg/L cyfluthrin + 10 µg/L copper mixture for 96 h. Cyfluthrin-exposed samples showed apparent vacuolization, basal lamina separations, and disrupted digestive cells. Exposure to copper alone gave rise to enlargements of the tubule lumens and the intertubular area, degenerated tubules, atrophied basophilic cells, prominently disrupted and ruptured digestive cells, and nuclear enlargements in some basophilic cells. Cyfluthrin and copper mixture caused more severe histopathological changes in the digestive gland. General tissue appearance was altered by prominently degenerated, and fused tubules lacking cellular structure; tubule lumens filled with cellular content were noted. Increased intertubular regions were filled with connective tissue formations. Progressive disruption of digestive cells; and basophilic cell atrophy were also observed. The findings of the current study highlighted that cyfluthrin and copper at environmentally relevant concentrations caused a biological response in L. stagnalis; however, this response was more intense following their co-exposure.

Keywords

Pyrethroid, heavy metal, toxicity, histopathology, snail

References

• [1] Ö. Fırat, H. Y. Cogun, T. A. Yüzereroğlu, G. Gök, Ö. Fırat, F. Kargin, Y. Kötemen, “A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus,” Fish Physiology and Biochemistry, vol. 37, no. 3, pp. 657-666, 2011.
• [2] H. Mai, J. Cachot, C. Clérandeau, C. Martin, N. Mazzela, P. Gonzalez, B. Morin, “An environmentally realistic pesticide and copper mixture impacts embryonic development and DNA integrity of the Pacific oyster, Crassostrea gigas,” Environmental Science and Pollution Research, vol. 27, no. 4, pp. 3600-3611, 2020.
• [3] P. Amoatey, M. S. Baawain, “Effects of pollution on freshwater aquatic organisms,” Water Environment Research, vol. 91, no. 10, pp 1272-1287, 2019.
• [4] C. A. Flemming, J. T. Trevors, “Copper toxicity and chemistry in the environment: a review,” Water, Air, and Soil Pollution, vol. 44, no. 1, pp. 143-158, 1989.
• [5] M. B. Jorge, V. L. Loro, A. Bianchini, C. M. Wood, P. L. Gillis, “Mortality, bioaccumulation and physiological responses in juvenile freshwater mussels (Lampsilis siliquoidea) chronically exposed to copper,” Aquatic Toxicology, vol. 126, pp. 137-147, 2013.
• [6] J. Bao, Y. Xing, C. Feng, S. Kou, H. Jiang, X. Li, “Acute and sub-chronic effects of copper on survival, respiratory metabolism, and metal accumulation in Cambaroides dauricus,” Scientific Reports, vol. 10, pp. 16700, 2020.
• [7] M. E. Tesser, A. A. de Paula, W. E. Risso, R. A. Monteiro, A. D. E. Santo Pereira, L. F. Fraceto, C. B. dos Reis Martinez, “Sublethal effects of waterborne copper and copper nanoparticles on the freshwater Neotropical teleost Prochilodus lineatus: A comparative approach,” Science of The Total Environment, vol. 704, pp. 135332, 2020.
• [8] J. L. Stauber, C. M. Davies, “Use and limitations of microbial bioassays for assessing copper bioavailability in the aquatic environment,” Environmental Reviews, vol. 8, no. 4, pp. 255-301, 2000.
• [9] M. D. Baldissera, C. F. Souza, D. C. Barroso, R. S. Pereira, K. O. Alessio, C. Bizzi, B. Baldisserotto, A. L. Val, “Acute exposure to environmentally relevant concentrations of copper affects branchial and hepatic phosphoryl transfer network of Cichlasoma amazonarum: Impacts on bioenergetics homeostasis,” Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, vol. 238, pp. 108846, 2020.
• [10] B. Das, R. Nordin, A. Mazumder, “Watershed land use as a determinant of metal concentrations in freshwater systems,” Environmental Geochemistry and Health, vol. 31, no. 6, pp. 595-607, 2009.
• [11] A. Sepici-Dinçel, A. Ç. K. Benli, M. Selvi, R. Sarıkaya, D. Şahin, I. A. Özkul, F. Erkoç, “Sublethal cyfluthrin toxicity to carp (Cyprinus carpio L.) fingerlings: biochemical, hematological, histopathological alterations,” Ecotoxicology and Environmental Safety, vol. 72, no. 5, pp. 1433-1439, 2009.
• [12] L. Li, D. Yang, Y. Song, Y. Shi, B. Huang, A. Bitsch, J. Yan, “The potential acute and chronic toxicity of cyfluthrin on the soil model organism, Eisenia fetida,” Ecotoxicology and Environmental Safety, vol. 144, pp. 456-463, 2017.
• [13] E. G. Günde, S. V. Yerli, “A comparative study on the acute toxicity of cyfluthrin and tetramethrin on carp (Cyprinus carpio L. 1758),” Journal of the Black Sea/Mediterranean Environment, vol. 17, pp. 260-268, 2011.
• [14] A. J. Thatheyus, A. G. Selvam, “Synthetic pyrethroids: toxicity and biodegradation,” Applied Ecology and Environmental Sciences, vol. 1, no. 3, pp. 33-36, 2013.
• [15] S. M. Brander, I. Werner, J. W. White, L. A. Deanovic, “Toxicity of a dissolved pyrethroid mixture to Hyalella azteca at environmentally relevant concentrations,” Environmental Toxicology and Chemistry: An International Journal, vol. 28, no. 7, pp. 1493-1499, 2009.
• [16] S. Zheng, B. Chen, X. Qiu, M. Chen, Z. Ma, X. Yu, “Distribution and risk assessment of 82 pesticides in Jiulong River and estuary in South China,” Chemosphere, vol. 144, pp. 1177-1192, 2016.
• [17] P. Arslan, “Determinations of the effects of cyfluthrin on the hemocytes parameters of freshwater mussel (Unio delicatus),” Ege Journal of Fisheries and Aquatic Sciences, vol. 39, no. 1, 39-45, 2022.
• [18] M. Lanteigne, S. A. Whiting, M. J. Lydy, “Mixture toxicity of imidacloprid and cyfluthrin to two non-target species, the fathead minnow Pimephales promelas and the amphipod Hyalella azteca,” Archives of Environmental Contamination and Toxicology, vol. 68, no. 2, pp. 354-361, 2015.
• [19] J. Amorim, I. Abreu, P. Rodrigues, D. Peixoto, C. Pinheiro, A. Saraiva, A. P. Carvalho, L. Guimarāes, L. Oliva-Teles, “Lymnaea stagnalis as a freshwater model invertebrate for ecotoxicological studies,” Science of the Total Environment, vol. 669, pp. 11-28, 2019.
• [20] R. Kuroda, M. Abe, “The pond snail Lymnaea stagnalis,” EvoDevo, vol. 11, no. 1, pp 1-10, 2020.
• [21] S. B. Karakaş, B. Otludil, “Accumulation and histopathological effects of cadmium on the great pond snail Lymnaea stagnalis Linnaeus, 1758 (Gastropoda: Pulmonata),” Environmental Toxicology and Pharmacology, vol. 78, pp. 103403, 2020.
• [22] R. W. Zurawell, J. I. Goldberg, C. F. Holmes, E. E. Prepas, “Tissue distribution and oral dose effects of microcystin in the freshwater pulmonate snail Lymnaea stagnalis jugularis (Say),” Journal of Toxicology and Environmental Health, Part A, vol. 70, no. 7, pp. 620-626, 2007.
• [23] J. Lajtner, R. Erben, G. I. Klobucar, “Histopathological effects of phenol on the digestive gland of Amphimelania holandri Fér. (Gastropoda, Prosobranchia),” Bulletin of Environmental Contamination and Toxicology, vol. 57, no. 3, pp. 458-464 1996.
• [24] B. Otludil, E. I. Cengiz, M. Z. Yildirim, Ö. Ünver, E. Ünlü, “The effects of endosulfan on the great ramshorn snail Planorbarius corneus (Gastropoda, Pulmonata): a histopathological study,” Chemosphere, vol. 56, no. 7, pp. 707-716, 2004.
• [25] E. Ünlü, E. I. Cengiz, M. Z. Yildirim, B. Otludil, Ö. Ünver, “Histopathological effects in tissues of snail Lymnaea stagnalis (Gastropoda, Pulmonata) exposed to sublethal concentration of Thiodan® and recovery after exposure,” Journal of Applied Toxicology, vol. 25, no. 6, pp. 459-463, 2005.
• [26] J. Murakami, R. Okada, H. Sadamoto, S. Kobayashi, K. Mita, Y. Sakamoto, M. Yamagishi, D. Hatakeyama, E. Otsuka, A. Okuta, H. Sunada, S. Takigami, M. Sakakibara, Y. Fujito, M. Awaji, S. Moriyama, K. Lukowiak, E. Ito, “Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis,”.Journal of Neuroscience, vol. 33, no. 1, pp. 371-383, 2013.
• [27] N. Akhtar, M. I. Syakir Ishak, S. A. Bhawani, K. Umar, “Various natural and anthropogenic factors responsible for water quality degradation: A review,” Water, vol. 13, no. 19, pp. 2660, 2021.
• [28] C. de Perre, T. M. Murphy, M. J. Lydy, “Mixture toxicity of phostebupirim and cyfluthrin: Species‐specific responses,” Environmental Toxicology and Chemistry, vol. 36, no. 7, pp. 1947-1954, 2017.
• [29] I. H. Baek, Y. Kim, S. Baik, J. Kim, “Investigation of the synergistic toxicity of binary mixtures of pesticides and pharmaceuticals on Aliivibrio fischeri in major river basins in South Korea,” International journal of Environmental Research and Public Health, vol. 16, no. 2, pp. 208, 2019.
• [30] C. Wang, Y. Yang, N. Wu, M. Gao, Y. Tan, “Combined toxicity of pyrethroid insecticides and heavy metals: a review,” Environmental Chemistry Letters, vol. 17, no. 4, pp. 1693-1706, 2019.
• [31] H. Zhang, X. Hong, S. Yan, J. Zha, J. Qin, “Environmentally relevant concentrations of bifenthrin induce changes in behaviour, biomarkers, histological characteristics, and the transcriptome in Corbicula fluminea,” Science of The Total Environment, vol. 728, pp. 138821, 2020.
• [32] F. Arrighetti, E. Ambrosio, M. Astiz, A. R. Capítulo, S. Lavarías, “Differential response between histological and biochemical biomarkers in the apple snail Pomacea canaliculata (Gasteropoda: Amullariidae) exposed to cypermethrin,” Aquatic Toxicology, vol. 194, pp. 140-151, 2018.
• [33] K. V. Brix, A. J. Esbaugh, M. Grosell, “The toxicity and physiological effects of copper on the freshwater pulmonate snail, Lymnaea stagnalis,” Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, vol. 154, no. 3, pp. 261-267, 2011.
• [34] A. Weber, M. von Randow, A. L. Voigt, M. von der Au, E. Fischer, B. Meermann, M. Wagner, “Ingestion and toxicity of microplastics in the freshwater gastropod Lymnaea stagnalis: No microplastic-induced effects alone or in combination with copper,” Chemosphere, vol. 263, pp. 128040, 2021.
• [35] G. Atli, M. Grosell, “Characterization and response of antioxidant systems in the tissues of the freshwater pond snail (Lymnaea stagnalis) during acute copper exposure,” Aquatic Toxicology, vol. 176, pp. 38-44, 2016.
• [36] J. A. Adeyemi, O. O. Adewale, A. Y. Oguma, “Mortality, oxidative stress and hepatotoxicity in juvenile African catfish, Clarias gariepinus Burchell, exposed to lead and cypermethrin,” Bulletin of Environmental Contamination and Toxicology, vol. 92, no. 5, pp. 529-533, 2014.
• [37] Y. Yang, X. Ye, B. He, J. Liu, “Cadmium potentiates toxicity of cypermethrin in zebrafish,” Environmental Toxicology and Chemistry, vol. 35, no. 2, pp. 435-445, 2016.
• [38] H. Rehman, A. T. Aziz, S. Saggu, A. L. VanWert, N. Zidan, S. Saggu, “Additive toxic effect of deltamethrin and cadmium on hepatic, hematological, and immunological parameters in mice,” Toxicology and Industrial Health, vol. 33, no. 6, pp. 495-502, 2017.