Influence of temperature on the antioxidant responses and lipid peroxidation of two species of tadpoles (Rhinella schneideri and Physalaemus nattereri) exposed to the herbicide sulfentrazone (Boral 500SC®)

Abstract

Amphibians can experience large temperature fluctuations in their habitats, especially during the larval stage, when tadpoles are restricted to small and ephemeral ponds. Changes in water temperature can alter development, metabolism and behaviour of cold-blooded animals but also the toxicokinetics of chemicals in the environment. In Brazil, pesticides application is intensified during the rainy season, which is the period of reproduction for many amphibian species. We evaluated here the influence of temperature (28, 32, and 36°C) on the toxicity of the herbicide sulfentrazone (Boral®SC) in tadpoles of Physalaemus nattereri and Rhinella schneideri, by analysis of oxidative stress biomarkers. Exposure of tadpoles to sulfentrazone altered the antioxidant enzymes activities and induced lipid peroxidation with temperature-associated responses. Catalase, superoxide dismutase and glucose-6-phosphate dehydrogenase (G6PDH) were impaired by combined effect of temperature and sulfentrazone in both species. G6PDH was increased in most groups exposed to 36°C. Biotransformation enzyme glutathione-S-transferase had more evident alterations in P. nattereri at higher temperatures and changes in tGSH contents presented different patterns between the species. Lipid peroxidation was particularly induced in tadpoles of P. nattereri. Integrated biomarker response (IBR) index indicated a synergic effect of temperature and sulfentrazone for tadpoles of P. nattereri, while the IBR was mainly influenced by temperature in R. schneideri. Our study showed that temperature modulates biochemical responses in tadpoles exposed to sulfentrazone with a species-specific pattern. These findings imply that the effects of abiotic factors should be taken into account to evaluate the real risks of exposure of amphibians to commonly used pesticides.

Effects of ecologically relevant concentrations of Boral® 500 SC, Glifosato® Biocarb, and a blend of both herbicides on markers of metabolism, stress, and nutritional condition factors in bullfrog tadpoles

“…Studies report possible herbicide concentrations that may be available in aquatic habitats after leaching (Thorngren et al 2017). Freitas et al (2017) used Boral® 500 SC-sulfentrazone concentrations of 10, 50, and 100 μg/L in exposure experiments using Rhinella schneideri and Physalaemus nattereri tadpoles.…”

“…The authors demonstrated that energetic reserves (glycogen, lipids, triglycerides, and proteins) of gills, liver, and muscles were completely depleted. Freitas et al (2017), performed one of the few studies about the effects of Boral® 500SC (active ingredient-sulfentrazone) on amphibians. The authors evaluated the influence of different temperatures (28, 32, and 36 °C) and concentrations of sulfentrazone (10, 50, and 100 μg/L) in Physalaemus nattereri and Rhinella schneider tadpoles in oxidative stress biomarkers.…”

“…Oxidative stress may cause enzymatic inactivity, DNA/RNA damage, macromolecules oxidation, cellular apoptosis, mutagenesis, carcinogenesis, among other alterations (Costantini 2014;Jones et al 2010;Lushchak and Bagnyukova 2006). Cases of oxidative stress caused by herbicide exposure have been recorded in different larval stages of amphibians (Coltro et al 2017;Costa et al 2008;Dornelles and Oliveira, 2014;Freitas et al 2017;Gripp et al 2017;Lajmanovich et al 2011;Yin et al 2014).…”

Integrative Biomarker Assessment of the Influence of Saxitoxin on Marine Bivalves: A Comparative Study of the Two Bivalve Species Oysters, Crassostrea gigas, and Scallops, Chlamys farreri

“…As a phase II detoxification enzyme, GST protects cells and tissues against oxidative stress by catalyzing the conjugation of the reduced form of glutathione to various xenobiotic substrates ( Hayes and Strange, 1995 ). The above-mentioned antioxidant enzyme activities alteration has been widely used as biochemical biomarkers for oxidative stress caused by environmental stressors ( Matozzo et al, 2013 ; Nogueira et al, 2015 ; Freitas et al, 2017 ). Based on this study, antioxidant enzymes (CAT, SOD, and GST) were generally stimulated in the digestive glands of both oysters and scallops, indicating that the antioxidant system was activated in response to the induction of oxidative stress caused by STX exposure.…”

Melanophryniscus admirabilis tadpoles’ responses to sulfentrazone and glyphosate-based herbicides: an approach on metabolism and antioxidant defenses

“…There are few studies on the effects of sulfentrazone in nontarget aquatic species other than those conducted by the US Environmental Protection Agency (USEPA) for sulfentrazone, and these studies indicate that nontarget aquatic vascular plants are the most susceptible to sulfentrazone, followed by phytoplankton, aquatic invertebrates, and fish (Thorngren et al 2017). Sulfentrazone can have negative effects on amphibians, as evidenced by Freitas et al (2017) where the herbicide caused the disruption of the oxidative balance of two species of amphibians native to Brazil (Rhinella schneideri and Physalaemus nattereri). Wilkens et al ( 2019) also observed changes in the energy reserves, plasma corticosterone, and oxidative balance of bullfrog tadpoles (Rana catesbeiana) exposed to Boral® 500SC.…”