High temperature aggravates the effects of pesticides in goldfish

Abstract

In human-altered rivers, fish are often conjointly exposed to an increase in water temperature due to global warming and to contamination by organic pollutants such as pesticides, but their combined effects are still elusive. Thermal and chemical stressors could potentially interact because high temperature increases metabolism and toxicant uptake, and can alter the ability of organisms to set up adequate stress responses and to maintain homeostasis. These combined stressors could thus potentially result in higher level of molecular and cellular damage, and stronger effects on behavior and physiology, but experimental evidence across biological levels is still scarce. In this study, goldfish Carassius auratus were experimentally exposed to an environmentally realistic cocktail of pesticides (S-metolachlor, isoproturon, linuron, atrazinedesethyl, aclonifen, pendimethalin and tebuconazol) commonly found in rivers of South-West of France at low or high dose in two different thermal conditions: a common summer temperature (22°C) or a high temperature recorded during heat waves (32°C). Results showed that high temperature alone caused behavioral and physiological changes (increased swimming activity, increased hepatosomatic index, decreased reproductive index) but limited cellular damage. However, high temperature aggravated the effects of pesticides at the molecular and cellular level. Indeed, pesticide exposure resulted in higher genotoxic effects (micronuclei rate) and irreversible cellular damage of the gills and liver (apoptosis, inflammation, necrosis) at 32°C compared to 22°C. This suggests potential synergic effects of climate change and pollution, and highlights the need for multiple stress approaches to better predict the impacts of human activities on aquatic wildlife.

Effects of Pollution on Fish Behavior, Personality, and Cognition: Some Research Perspectives

“…Other stressors such as climate change and water warming could also modulate the effects of pollutants, either through direct effects on the chemical properties of pollutants, and/or through complex interactive effects on neurophysiological pathways (Schiedek et al, 2007;Noyes et al, 2009). For instance, exposure to pesticides and water warming in goldfish had complex interactive effects on goldfish Carassius auratus proteome and cell integrity (Gandar et al, 2017b;Jacquin et al, 2019), and resulted in antagonistic effects on fish foraging activity in fish exposed to multiple stressors compared to fish exposed to single stressors (Gandar et al, 2015). To conclude, pollution effects often depend on the concomitant exposure to other biotic and abiotic stressors (Dinh Van et al, 2013Tüzün et al, 2015Tüzün et al, , 2017Debecker and Stoks, 2019;Saaristo et al, 2019), underlining the need for multistress approaches to better predict the cognitive and fitness consequences of pollution on wildlife.…”

Direct and indirect effects of multiple environmental stressors on fish health in human-altered rivers

“…Liver lesions were quantified by standard histological techniques following previous studies in fish (Cuevas et al, 2016;Jacquin et al, 2019;van Dyk et al, 2007). Briefly, the liver was dissected, immediately fixed in 4% formalin, and then paraffin-embedded.…”

“…For each hepatic lesion, a score between 0 and 3 was associated according to the severity of the lesion. A global histopathological score reflecting the severity of the lesions was then calculated as the mean value of the different scores following previous studies (Jacquin et al, 2019).…”

“…Multiple stressors may also have complex interactive effects on detoxification processes and contaminants bioaccumulation, and trigger inflammatory responses, oxidative stress and cellular damage depending on the combination of stressors. For instance, high temperature can aggravate the effects of contamination by increasing fish metabolism and contaminants uptake (Guinot et al, 2012;Noyes et al, 2009;Sokolova and Lannig, 2008) and may result in higher oxidative stress and cellular lesions (Gandar et al, 2017b;Jacquin et al, 2019). In addition, the activation of costly immune and inflammatory responses under multiple stress is expected to affect energy management and deplete energy reserves (Gimbo et al, 2015;Marteinson et al, 2017;Martin et al, 2003), thereby affecting fish body condition and growth at the individual level (Johnson and Dick, 2001;Jokela and Mutikainen, 1995;Wernicke von Siebenthal et al, 2018).…”

How Do Indirect Effects of Contaminants Inform Ecotoxicology? A Review

“…For example, environmental factors such as temperature may alter the effects of toxicants on behavior. Jacquin et al [36] found that high temperatures aggravated the effects of pesticides in goldfish, and Lagesson et al [37] found that exposure to a hormonal growth promoter increased boldness behavior in mosquitofish, but that this increase depended on temperature. Araujo et al [38] observed that shrimps balanced exposure to contaminants with a sheltering behavior that protects individuals from predators; when confronted with a choice between a cleaner habitat with no shelter and a contaminated habitat with shelter, shrimps preferred the cleanest area, but when the uncontaminated area contained a predator signal, shrimps balanced the risk of predation and exposure to contamination by selecting a moderately contaminated area further away from predator signals, thereby increasing their exposure to the contaminant.…”