Abstract
Abamectin is one of the most used pesticides worldwide. However, investigations about its effects on amphibian populations are rare. Thus, the present study sought to investigate possible cytotoxic effects on Lithobates catesbeianus tadpoles exposed to low abamectin concentrations diluted in water. Accordingly, four experimental groups were set: negative control, positive control (cyclophosphamide—40 mL L−1), abamectin at concentrations 36 μg a.i./L (ABA36 group), and 72 μg a.i./L (ABA72 group), applied as Kraft® 36EC. The micronucleus test was conducted and other nuclear abnormalities in peripheral blood erythrocytes were checked after 24, 48, and 72 h of exposure to the treatments. The total of other nuclear abnormalities was influenced by the treatments, whereas the frequency of micronuclei was influenced by the exposure time. Such frequency was higher in the animals comprising the ABA72 group, which was assessed 72 h after the exposure had begun. The total of other nuclear abnormalities was influenced by the treatments. Animals in the positive control, ABA36, and ABA72 groups showed similar frequency of these abnormalities at 48 and 72 h. However, this frequency was statistically higher than that of animals in their respective negative control groups. Thus, the present study confirmed the hypothesis that the exposure of L. catesbeianus tadpoles to abamectin caused cytotoxic effects on them, although this exposure lasted short and the concentrations were low. It disclosed prospects for variations in the nucleus of erythrocytes circulating in amphibians, a fact that may provide an important/complementary approach for the detection of cytotoxicity caused by abamectin exposure.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Akar MW, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–2. https://doi.org/10.2478/v10102-009-0001-7
Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJA, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci Process Impacts 18:779–787. https://doi.org/10.1039/c6em00268d
Al-Sarar AS, Abobakr Y, Bayoumi AE, Hussein HI (2015) Cytotoxic and genotoxic effects of abamectin, chlorfenapyr, and imidacloprid on CHOK1 cells. Environ Sci Pollut Res 22:17041–17052. https://doi.org/10.1007/s11356-015-4927-3
American Society for Testing and Materials (ASTM) (2004) Active standard: E1439-98. Standard guide for conducting the frog embryo teratogenisis assay-Xenopus (FETAX), 16p
Bai SH, Ogbourne S (2016) Eco-toxicological effects of the avermectin family with a focus on abamectin and ivermectin. Chemosphere 154:204–214. https://doi.org/10.1016/j.chemosphere.2016.03.113
Bosch B, Mañas F, Gorla N, Aiassa D (2011) Micronucleus test in post metamorphic Odontophrynus cordobae and Rhinella arenarum (Amphibia: Anura) for environmental monitoring. J Toxicol Environ Health Sci 3:155–163
Bridges CM, Dwyer FJ, Hardesty DK, Whites DW (2002) Comparative contaminant toxicity: are amphibian larvae more sensitive than fish? Bull Environ Contam Toxicol 69:562–569. https://doi.org/10.1007/s00128-002-0098-2
Campbell WC (2012) Ivermectin and abamectin. Springer Science & Business Media, Berlin
Carbonell E, Valbuena A, Xamena N, Creus A, Marcos R (1995) Temporary variations in chromosomal aberrations in a group of agricultural workers exposed to pesticides. Mutat Res 344:127–134. https://doi.org/10.1016/0165-1218(95)00051-8
Casali-Pereira MP, Daam MA, de Resende JC, Vasconcelos AM, Espíndola EL, Botta CM (2015) Toxicity of Vertimec® 18 EC (active ingredient abamectin) to the neotropical cladoceran Ceriodaphnia silvestrii. Chemosphere 139:558–564. https://doi.org/10.1016/j.chemosphere.2015.08.006
Crane M, Finnegan M, Weltje L, Kosmala-Grzechnik S, Gross M, Wheeler JR (2016) Acute oral toxicity of chemicals in terrestrial life stages of amphibians: comparisons to birds and mammals. Regul Toxicol Pharmacol 80:335–341. https://doi.org/10.1016/j.yrtph.2016.05.004
Egea-Serrano A, Relyea RA, Tejedo M, Torralva M (2012) Understanding the impact of chemicals on amphibians: a meta-analytic review. Ecol Evol 2:1382–1397. https://doi.org/10.1002/ece3.249
el-Ashmawy IM, el-Nahas AF, Bayad AE (2011) Teratogenic and cytogenetic effects of ivermectin and its interaction with P-glycoprotein inhibitor. Res Vet Sci 90:116–123. https://doi.org/10.1016/j.rvsc.2010.05.020
Environmental Protection Agency US (EPA) (1989) Avermectin (Agri-Mek, Affirm) pesticide fact sheet 9/89. Cornell University
Freitas JS, Kupsco AJ, Diamante G, Felicio AA, Alves de Almeida E, Schlenk D (2016) Influence of temperature on the thyroidogenic effects of Diuron and its metabolite 3,4-DCA in tadpoles of the American bullfrog (Lithobates catesbeianus). Environ Sci Technol 50:13095–13104. https://doi.org/10.1021/acs.est.6b04076
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Perspect 111:568–575
Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755. https://doi.org/10.1038/35008052
Jensen J, Diao X, Scott-fordsmand JJ (2007) Sub-lethal toxicity of the antiparasitic abamectin on earthworms and the application of neutral red retention time as a biomarker. Chemosphere 68:744–750. https://doi.org/10.1016/j.chemosphere.2006.12.094
Krieger R (2001) Handbook of pesticide toxicology, two-volume set: principles and agents, vol 1. Academic Press, Cambridge
Lajmanovich RC, Cabagna-Zenklusen MC, Attademo AM, Junges CM, Peltzer PM, Bassó A, Lorenzatti E (2014) Induction of micronuclei and nuclear abnormalities in tadpoles of the common toad (Rhinella arenarum) treated with the herbicides Liberty® and glufosinate-ammonium. Mutat Res Genet Toxicol Environ Mutagen 769:7–12. https://doi.org/10.1016/j.mrgentox.2014.04.009
Lips KR (1998) Decline of a tropical montane amphibian fauna. Conserv Biol 12:106–112. https://doi.org/10.1111/j.1523-1739.1998.96359.x
Lovel DP (2013) Draft report on statistical issues related to OECD in vitro genotoxicity test guidelines. Available in: http://www.oecd.org/env/ehs/testing/Stat%20report%20TG%20473_487.pdf. Access on: 15 Nov 2016
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. https://doi.org/10.1016/j.envpol.2009.05.015
Molinari G, Soloneski S, Reigosa MA, Larramendy ML (2009) In vitro genotoxic and cytotoxic effects of ivermectin and its formulation ivomec on Chinese hamster ovary (CHOK1) cells. J Hazard Mater 165:1074–1082. https://doi.org/10.1016/j.jhazmat.2008.10.083
Molinari G, Soloneski S, Larramendy ML (2010a) New ventures in the genotóxico and cytotoxic effects of macrocyclic lactones, abamectin and ivermectin. Cytogenet Genome Res 128:37–45
Molinari G, Soloneski S, Reigosa MA, Larramendy ML (2010b) Genotoxic and cytotoxic in vitro evaluation of ivermectin and its formulation Ivomec® on Aedes albopictus larvae (CCL-126™) cells. Toxicol Environ Chem 92:1577–1593. https://doi.org/10.1080/02772241003625284
Molinari G, Kujawski M, Scuto A, Soloneski S, Larramendy ML (2013) DNA damage kinetics and apoptosis in ivermectin-treated Chinese hamster ovary cells. J Appl Toxicol 33:1260–1267. https://doi.org/10.1002/jat.2782
Novelli A, Vieira BH, Cordeiro D, Cappelini LT, Vieira EM, Espíndola EL (2012a) Lethal effects of abamectin on the aquatic organisms Daphnia similis, Chironomus xanthus and Danio rerio. Chemosphere 86:36–40. https://doi.org/10.1016/j.chemosphere.2011.08.047
Novelli A, Vieira BH, Vasconcelos AM, Peret AC, Epíndola ELG (2012b) Field and laboratory studies to assess the effects of Vertimec (R) 18EC on Daphnia similis. Ecotoxicol Environ Saf 75:87–93. https://doi.org/10.1016/j.ecoenv.2011.08.016
Novelli A, Vieira BH, Braun AS, Mendes LB, Daam MA, Espíndola EL (2016) Impact of runoff water from an experimental agricultural field applied with Vertimec® 18EC (abamectin) on the survival, growth and gill morphology of zebrafish juveniles. Chemosphere 144:1408–1414. https://doi.org/10.1016/j.chemosphere.2015.10.004
Ossana NA, Salibián A (2013) Micronucleus test for monitoring the genotoxic potential of the surface water of Luján River (Argentina) using erythrocytes of Lithobates catesbeianus tadpoles. Ecotoxicol Environ Contam 8:67–74. https://doi.org/10.5132/eec.2013.01.010
Rissoli RZ, Abdalla FC, Costa MJ, Rantin FT, McKenzie DJ, Kalinin AL (2016) Effects of glyphosate and the glyphosate based herbicides Roundup Original(®) and Roundup Transorb(®) on respiratory morphophysiology of bullfrog tadpoles. Chemosphere 156:37–44. https://doi.org/10.1016/j.chemosphere.2016.04.083
Sankoh AI, Whittle R, Semple KT, Jones KC, Sweetman AJ (2016) An assessment of the impacts of pesticide use on the environment and health of rice farmers in Sierra Leone. Environ Int 94:458–466. https://doi.org/10.1016/j.envint.2016.05.034
Shoop WL, Mrozik H, Fisher MH (1995) Structure and activity of avermectins and milbemycins in animal health. Vet Parasitol 59:139–156. https://doi.org/10.1016/0304-4017(94)00743-V
Silva Mdos S, Cocenza DS, Grillo R, de Melo NF, Tonello PS, de Oliveira LC, Cassimiro DL, Rosa AH, Fraceto LF (2011) Paraquat-loaded alginate/chitosan nanoparticles: preparation, characterization and soil sorption studies. J Hazard Mater 190:366–374. https://doi.org/10.1016/j.jhazmat.2011.03.057
Sparling DW, Fellers GM (2009) Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environ Toxicol Chem 28(8):1696–1703. https://doi.org/10.1897/08-336.1
Tisler T, Kozuh Erzen N (2006) Abamectin in the aquatic environment. Ecotoxicology 15:495–502. https://doi.org/10.1007/s10646-006-0085-1
United States Environmental Protection Agency (USEPA) (2002) Methods for evaluating wetland and condition: using amphibians in bioassessments of wetlands. EPA-822-R-02-022. Environmental Protection Agency, 41p
Vasconcelos AM, Daam M, Santos LRA, Sanches ALM, Araújo CVM, Espíndola ELG (2016) Acute and chronic sensitivity, avoidance behavior and sensitive life stages of bullfrog tadpoles exposed to the biopesticide abamectin. Ecotoxicology 25:500–509. https://doi.org/10.1007/s10646-015-1608-4
Veronez AC, Salla RV, Baroni VD, Barcarolli IF, Bianchini A, Dos Reis Martinez CB, Chippari-Gomes AR (2016) Genetic and biochemical effects induced by iron ore, Fe and Mn exposure in tadpoles of the bullfrog Lithobates catesbeianus. Aquat Toxicol 174:101–108. https://doi.org/10.1016/j.aquatox.2016.02.011
Wilson C, Tisdell C (2001) Why farmers continue to use pesticides despite environmental, health and sustainability costs. Ecol Econ 39:449–462. https://doi.org/10.1016/S0921-8009(01)00238-5
Wirz MV, Saldiva PH, Freire-Maia DV (2005) Micronucleus test for monitoring genotoxicity of polluted river water in Rana catesbeiana tadpoles. Bull Environ Contam Toxicol 75:1220–1227. https://doi.org/10.1007/s00128-005-0879-5
Xu Y, Zhang S, Zhang Y, Hu J, Bhattacharya H (2005) Exposure of rosy barb (Puntius conchonius) sperm to abamectin as an in vitro assay of cytotoxicity. Toxicol Mech Methods 15:351–354. https://doi.org/10.1080/15376520500194684
Zahid HJ, Robinson E, Kelly RL (2016) Agriculture, population growth, and statistical analysis of the radiocarbon record. PNAS 113:931–935. https://doi.org/10.1073/pnas.1517650112
Acknowledgments
The authors are grateful to the Brazilian National Council for Research (CNPq) (Brazilian research agency) (Proc. No. 467801/2014-2) and Instituto Federal Goiano for the financial support. Moreover, the authors are grateful to the CNPq for supporting scholarship to the student who developed this study.
Funding
This study was funded by the Brazilian National Council for Research (CNPq) (Brazilian research agency) (Proc. No. 467801/2014–2) and Instituto Federal Goiano—Campus Urutaí (GO, Brazil).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All the procedures were approved by The Ethics Committee on Animal Use of Goiano Federal Institute (Comissão de Ética no Uso de Animais do Instituto Federal Goiano), GO, Brazil (Protocol No. 6181130516/2016). Meticulous efforts were made to assure that the animals suffered the least possible and to reduce external sources of stress, pain, and discomfort. The current study did not exceed the number of animals necessary to produce trustworthy scientific data. This article does not contain any studies with human participants performed by any of the authors.
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Montalvão, M.F., Malafaia, G. Effects of abamectin on bullfrog tadpoles: insights on cytotoxicity. Environ Sci Pollut Res 24, 23411–23416 (2017). https://doi.org/10.1007/s11356-017-0124-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-0124-x