Skip to main content
SpringerLink
Log in

Histopathologic and genotoxic effects of deltamethrin on marsh frog, Pelophylax ridibundus (Anura: Ranidae)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

It is known that amphibians inhabiting agricultural areas are constantly exposed to chemicals such as insecticides. Deltamethrin, a type II pyrethroid insecticide, is widely used in the world. The present study aimed to investigate the toxic effects of different concentrations (0.625, 1.25, and 2.50 mg/kg body wt) of orally applied deltamethrin to marsh frog (Pelophylax ridibundus) after 96 h of treatment. The histopathological abnormalities in liver, gastrointestinal tract, and kidney tissues were evaluated with quantitative analyses. In liver, increase of melanomacrophagic aggregates, non-homogeneous hepatocyte parenchyma, sinusoidal dilatations, infiltration, vascular epithelial degeneration, central vein degeneration, and congestion were determined in exposed frogs. In gastrointestinal tract, vacuolization, hypertrophy, congestion, infiltration, necrosis, and erosion of the epithelial layer, increasing goblet secretion, degeneration in villi, epithelial disorganization, and edema were observed in high-dose groups. In all experimental groups, glomerular shrinkage, hemorrhage, degeneration, infiltration, increase in Bowman distance, and eosinophilic-stained tubular lumens were detected in kidneys. Histopathological changes were more prominent in 1.25 and 2.50 mg/kg groups than the other groups. To determine the genotoxic effects of deltamethrin, the peripheral blood samples of the frogs were used. The erythrocytic nuclear abnormalities such as micro-nucleus, double-nucleus, kidney-shaped nucleus, notched nucleus, and bud nucleus were determined in the frogs, and the genotoxicity did not show a significant increase between control and low-dose groups, statistically. However, the genotoxic effects increased in medium- and especially high-dose groups. The results of this study showed that acute deltamethrin exposure can lead to histopathologic and genotoxic effects in P. ridibundus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abdel-Moneim AM, Al-Kahtani MA, Elmenshawy OM (2012) Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere 88:1028–1035

    Article  CAS  Google Scholar 

  • Alexander GJ, Horne D, Hanrahan SA (2002) An evaluation of the effects of deltamethrin on two non-target lizard species in the Karoo, South Africa. J Arid Environ 50:121–133

    Article  Google Scholar 

  • Ansari RA, Kaur M, Ahmad F, Rahman S, Rashid H, Islam F, Raisuddin S (2009) Genotoxic and oxidative stress-inducing effects of Deltamethrin in the erythrocytes of a freshwater biomarker fish species, Channa punctata Bloch. Environ Toxicol 24:429–436

    Article  CAS  Google Scholar 

  • Assis HCS, Nicareta L, Salvo LM, Klemz C, Truppel JH, Calegari R (2009) Biochemical biomarkers of exposure to deltamethrin in freshwater fish, Ancistrus multispinis. Braz Arch Biol Technol 52:1401–1407

    Article  Google Scholar 

  • Banerjee S, Bhattacharya S (1995) Histopathological changes induced by chronic nonlethal levels of elsan, mercury, and ammonia in the small intestine of Channa punctatus. Ecotoxicol Environ Saf 31:62–68

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W, Brkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34

    Article  Google Scholar 

  • Brühl CA, Pieper S, Weber B (2011) Amphibians at risk? Susceptibility of terrestrial amphibian life stages to pesticides. Environ Toxicol Chem 30:2465–2472

    Article  CAS  Google Scholar 

  • Çakıcı Ö (2014) Carbaryl-induced histopathologic alterations in the digestive tract of the levantine frog, Pelophylax bedriagae (Anura: Ranidae). Toxicol Pathol 42:1032–1040

    Article  CAS  Google Scholar 

  • Çakıcı Ö (2015) Histopathologic changes in liver and kidney tissues induced by carbaryl in Bufotes variabilis (Anura: Bufonidae). Environ Toxicol Pathol 67:237–243

    Article  CAS  Google Scholar 

  • Çakıcı Ö (2016) Histopathological study of toxic effects of carbaryl on digestive tract of Bufotes variabilis (Anura: Bufonidae). Environ Sci Pollut Res 23:13432–13437

    Article  CAS  Google Scholar 

  • Carrasco KR, Tilbury KL, Myers MS (1990) Assessment of the piscine micronuclei test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci 47:2123–2136

    Article  CAS  Google Scholar 

  • Çiçek K, Mermer A (2007) Food composition of the marsh frog, Rana ridibunda Pallas, 1771, in Thrace. Turk J Zool 31:83–90

    Google Scholar 

  • Datta M, Kaviraj A (2003) Acute toxicity of the synthetic pyrethroid deltamethrin to freshwater catfish Clarias gariepinus. Bull Environ Contam Toxicol 70:296–299

    Article  CAS  Google Scholar 

  • Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Deleguea M (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419

    Article  CAS  Google Scholar 

  • dos Santos Cunha F, da Costa Sousa N, Santos RFB, Meneses JO, do Couto MVS, de Almeida FTC, Fujimoto RY (2018) Deltamethrin-induced nuclear erythrocyte alteration and damage to the gills and liver of Colossoma macropomum. Environ Sci Pollut Res 25:15102–15110

    Article  CAS  Google Scholar 

  • DuRant SE, Hopkins WA, Talent LG (2007) Impaired terrestrial and arboreal locomotor performance in the western fence lizard (Sceloporus occidentalis) after exposure to an AChE-inhibiting pesticide. Environ Pollut 149:18–24

    Article  CAS  Google Scholar 

  • Ezemonye L, Tongo I (2010) Sublethal effects of endosulfan and diazinon pesticides on glutathione-S-transferase (GST) in various tissues of adult amphibians (Bufo regularis). Chemosphere 81:214–217

    Article  CAS  Google Scholar 

  • Froese JM, Smits JE, Forsyth DJ, Wickstrom ML (2009) Toxicity and immune system effects of dietary deltamethrin exposure in tiger salamanders (Ambystoma tigrinum). J Toxicol Environ Health A 72:518–526

    Article  CAS  Google Scholar 

  • Gonçalves MW, Carvalho WF, Pereira RR, Silva DM, Bastos RP, Cruz AD (2014) Avaliação de danos genômicos em anfíbios anuros do cerrado goiano. Estudos 41:89–104 (in Portuguese)

    Google Scholar 

  • Goulet NB, Hontella A (2003) Toxicity of cadmium, endosulfan and atrazine in adrenal steriodogenic cells of two amphibian species; Xenopus laevis and Rana catesbeiana. Environ Toxicol Chem 22:2106–2113

    Article  CAS  Google Scholar 

  • Haverinen J, Vornanen M (2016) Deltamethrin is toxic to the fish (crucian carp, Carassius carassius) heart. Pestic Biochem Physiol 129:36–42

    Article  CAS  Google Scholar 

  • Hopkins WA (2007) Amphibians as models for studying environmental change. ILAR J 48:270–277

    Article  CAS  Google Scholar 

  • IUCN (2009) Red list of threatened species. International Union for Conservation of Nature. https://doi.org/10.2305/IUCN.UK.2009.RLTS.T58705A11825745.en

  • Jayawardena UA, Angunawela P, Wickramasinghe DD, Ratnasooriya WD, Udagama PV (2017) Heavy metal–induced toxicity in the Indian green frog: Biochemical and histopathological alterations. Environ Toxicol Chem 36:2855–2867

    Article  CAS  Google Scholar 

  • Jha AN (2008) Ecotoxicological applications and significance of the comet assay. Mutagenesis 23:207–221

    Article  CAS  Google Scholar 

  • Köprücü SŞ, Yonar E, Seker E (2008) Effects of deltamethrin on antioxidant status and oxidative stress biomarkers in freshwater mussel, Unio elongatulus eucirrus. Bull Environ Contam Toxicol 81:253–257

    Article  CAS  Google Scholar 

  • Kumar A, Sasmal D, Sharma N (2015) An insight into deltamethrin induced apoptotic calcium, p53 and oxidative stress signalling pathways. Toxicol Environ Heal Sci 7:25–34

    Article  Google Scholar 

  • Li XY, Zeng SH, Zhang WH, Liu L, Ma S, Wang JJ (2013) Acute toxicity and superficial damage to goldfish from the ionic liquid 1-methyl-3 octylimidazolium bromide. Environ Toxicol 28:207–214

    Article  CAS  Google Scholar 

  • Lima CFM (2006) Effects of Salvia officinalis in the liver: relevance of glutathione levels. Universidade do Minho. p. 447 (Ph.D. thesis)

  • Macagnan N, Rutkoski CF, Kolcenti C, Vanzetto GV, Macagnan LP, Sturza PF, Hartmann PA, Hartmann MT (2017) Toxicity of cypermethrin and deltamethrin insecticides on embryos and larvae of Physalaemus gracilis (Anura: Leptodactylidae). Environ Sci Pollut Res 24:20699–20704

    Article  CAS  Google Scholar 

  • Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157:2903–2927

    Article  CAS  Google Scholar 

  • Marques SM, Antunes SC, Pissarra H, Pereira ML, Gonçalves F, Pereira R (2009) Histopathological changes and erythrocytic nuclear abnormalities in Iberian green frogs (Rana perezi Seoane) from a uranium mine pond. Aquat Toxicol 91:187–195

    Article  CAS  Google Scholar 

  • Marques A, Custódio M, Guilherme S, Gaivão I, Santos MA, Pacheco M (2014) Assessment of chromosomal damage induced by a deltamethrin-based insecticide in fish (Anguilla anguilla L.) - a follow-up study upon exposure and post-exposure periods. Pestic Biochem Physiol 113:40–46

    Article  CAS  Google Scholar 

  • Mollov I, Boyadzhiev P, Donev A (2010) Trophic role of the marsh frog Pelophylax ridibundus (Pallas, 1771) (Amphibia, Anura) in the aquatic ecosystems. Bulg J Agric Sci 16:298–306

    Google Scholar 

  • Mutschmann F (1991) Ectoparasite control with synthetic pyrethroids in reptiles. In: Internationales Kolloquium fur Pathologie und Therapie der Reptilien und Amphibien DVG-4. Deutsche Veterinarmedizinische Gesellschaft, Giessen, pp 95–106

    Google Scholar 

  • Özelmas U, Akay MT (1995) Histopathological investigations of the effects of malathion on dwarf lizards (Lacerta parva Boulenger 1887). Bull Environ Contam Toxicol 55:730–737

    Article  Google Scholar 

  • Parikh PH, Rangrez A, Adhikari Bagchi R, Desai BN (2010) Effect of Dimethoate on some histoarchitecture of freshwater fish Oreocromis mossambicus (Peters, 1852). Bioscan 5:55–58

    CAS  Google Scholar 

  • Parmar TK, Rawtani D, Agrawal YK (2016) Bioindicators: the natural indicator of environmental pollution. Front Life Sci 9:110–118

    Article  CAS  Google Scholar 

  • Păunescu A, Ponepal MC (2011) Nephrotoxic effects of Champions 50WP fungicides in the marsh frog Pelophylax ridibundus. Oltenia. Studii şi comunicări. Ştiinţele Naturii, Tom 27(1):119–122

  • Păunescu A, Ponepal CM, Drăghici O, Marinescu AG (2010a) Liver histopathologic alterations in the frog Rana (Pelophylax) ridibunda induce by the action of Reldan 40ec insecticide. Analele Universitatii din Oradea-Fascicula Biologie. Tom. XVII/1, pp. 166–169

  • Păunescu A, Ponepal C, Drăghici O, Marinescu AG (2010b) Histopathological responses of the liver tissues of Rana ridibunda to the Champions 50WP fungicide. Ann Food Sci Technol 11:60–64

    Google Scholar 

  • Păunescu A, Ponepal CM, Grigorean VT, Popescu M (2012) Histopathological changes in the liver and kidney tissues of Marsh Frog (Pelophylax ridibundus) induced by the action of Talstar 10EC insecticide. An U O Fasc Biol 19:5–10

  • Pimpão CT, Zampronio AR, de Assis HCS (2008) Exposure of Ancistrus multispinis (Regan, 1912, Pisces, Teleostei) to deltamethrin: effects on cellular immunity. Fish Shellfish Immunol 25:528–532

    Article  CAS  Google Scholar 

  • Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Muller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Fishing News Books, Oxford, pp 339–352

    Google Scholar 

  • Radovanović TB, Nasia M, Krizmanic II, Prokic MD, Gavric JP, Despotovic SG, Gavrilovic BR, Borkovic-Mitic SS, Pavlovic SZ, Saicic ZS (2017) Sublethal effects of the pyrethroid insecticide deltamethrin on oxidative stress parameters in green toad (Bufotes viridis L.). Environ Toxicol Chem 36:2814–2822

    Article  CAS  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad Sci U S A 98:2491–2496

    Article  CAS  Google Scholar 

  • Rendon-von Osten J, Ortiz-Arana A, Guilhermino L, Soares AM (2005) In vivo evaluation of three biomarkers in the mosquitofish (Gambusia yucatana) exposed to pesticides. Chemosphere 58:627–636

    Article  CAS  Google Scholar 

  • Renuka MR (2007) Effects of some pesticides on histopathological and biochemical aspects of Euphlyctis hexadactylus (Lesson) Amphibia: Anura. Ph.D. thesis, Mahatma Ghandi University, p. 150

  • Rybacki M, Berger L (1994) Distribution and ecology of water frogs in Poland. Zool Pol 39:293–303

    Google Scholar 

  • Şişman T, Keskin MÇ, Dane H, Adil Ş, Geyikoğlu F, Çolak S, Canpolat E (2020) Marsh frog (Pelophylax ridibundus) as a bioindicator to assess pollution in an agricultural area. Pak J Zool:1–13. https://doi.org/10.17582/journal.pjz/20190103130130

  • Soufy H, Soliman M, El-Manakhly E (2007) Some biochemical and pathological investigations on monosex Tilapia following chronic exposure to carbofuran pesticides. Glob Vet 1:45–52

    Google Scholar 

  • Stewart DAB, Seesink LD (1996) Impact of locust control in a semi-arid ecosystem in South Africa. Proceedings of the Brighton Crop Protection Conference: Pests and Diseases 3:1193–1198

  • Taylor B, Skelly D, Demarchis LK, Slade MD, Galusha D, Rabinowitz PM (2005) Proximity to pollution sources and risk of amphibian limb malformation. Environ Health Perspect 113:1497–1501

    Article  Google Scholar 

  • Van Meter RJ, Glinski DA, Henderson WM, Purucker ST (2015) Pesticide uptake across the amphibian dermis through soil and overspray exposures. Arch Environ Contam Toxicol 69:545–556

    Article  CAS  Google Scholar 

  • Velmurugan B, Selvanayagam M, Cengiz EI, Unlu E (2007) Histopathology of lambda-cyhalothrin on tissues (gill, kidney, liver and intestine) of Cirrhinus mrigala. Environ Toxicol Pharmacol 24:286–291

    Article  CAS  Google Scholar 

  • WHO (2010) WHO specifications and evaluations for public health pesticides- Deltamethrin. World Health Organization, Geneva

    Google Scholar 

Download references

Acknowledgments

We thank Dr. Şeymanur Adil for the experimental support.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ataturk University, 25240, Erzurum, Turkey

    Faten Alnoaimi, Hatice Dane & Turgay Şişman

Authors
  1. Faten Alnoaimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hatice Dane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Turgay Şişman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Turgay Şişman.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alnoaimi, F., Dane, H. & Şişman, T. Histopathologic and genotoxic effects of deltamethrin on marsh frog, Pelophylax ridibundus (Anura: Ranidae). Environ Sci Pollut Res 28, 3331–3343 (2021). https://doi.org/10.1007/s11356-020-10711-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10711-5

Keywords

Search

Navigation