Endocrine disrupting effects, at different temperatures, on Moina micrura (Cladocera: Crustacea) induced by carbendazim, a fungicide

Abstract

Pesticide-induced effects in non-target organisms are a worldwide environmental problem and cladocerans have been used as test organisms to quantify the toxicity effects. However, little is known about the true risks of acceptable levels, when non-traditional end points such as sex determination, egg maturation, and teratogenesis are considered. Aims of the present study were to investigate the effects of sublethal concentrations of the fungicide carbendazim taking into account the above-mentioned endpoints and to evaluate their sensitivity to an environmental factor such as temperature, known to influence growth rates and sex determination in cladocerans. We quantified the effect on the life history variables of Moina micrura at two different temperatures using the life table demographic approach, starting with neonates. The median lethal concentration of carbendazim for M. micrura was 0.12 ± 0.01 mg l−1. The impacts of carbendazim were assessed in experiments conducted at 20°C (experiment 1) and 30°C (experiment 3) using four sublethal concentrations of carbendazim (0.01, 0.02, and 0.04) and controls. An additional experiment (experiment 2) on the next generation (F1) was conducted at 20°C, using the offspring of the second clutches of M. micrura from each of the corresponding treatments of the experiment 1. The increase in temperature from 20 to 30°C significantly reduced always the average lifespan and life expectancy at birth, while raised the rate of population increase, net reproductive rate, and reproductive effort, in controls but not in carbendazim treatments. Higher temperature also increased male/female ratio. The patterns of survivorship curves were weakly affected by carbendazim exposure, but increase in concentration of this fungicide reduced offspring production, reproductive rates, and the rate of population increase, more noticeable at the higher temperature. These detrimental effects were much more striking in the F1 experiment, in which females were unable to produce viable offspring in the two highest carbendazim concentrations, although survival and swimming behavior were not significantly affected. This indicates that sensitivity to the toxicant is greater during egg development and that the fungicide acts as an endocrine disruptor. The presence of carbendazim in the medium resulted in higher male production as compared with controls, indicating also its effect on egg development. We also encountered a few individuals, with abnormal sexual secondary characters (males with reduced antennule length, similar to female antennules) at the highest carbendazim concentration. The role of carbendazim on the demography of cladocerans in natural systems, subject to temperature increase, is discussed taking into account the persistence of this chemical and its elevated impact in the successive generations (through the higher sensitivity of the developing eggs to the chemical at high temperatures). Cladoceran bioassays starting with neonates, which usually utilize offspring as sublethal endpoints should include the first generation to evaluate fecundity responses.