Insight into the Mechanism of Reproductive Dysfunction Caused by Neonicotinoid Pesticides

Abstract

Neonicotinoids, which were developed in the 1990 s as an insecticide having selective toxicity, were later found to cause reproductive abnormalities in experimental animals. In Japan there is an attempt to preserve endangered animals, including the Japanese crested ibis, and there is a question of whether neonicotinoids affect the reproduction of this bird, since they are used in its habitat. Hence, we investigated whether the daily oral administration of the neonicotinoid clothianidin (CTD) has any deleterious effects on the reproductive function of mature male only or both young male and female quails as experimental animals. Vacuolization and the number of germ cells having fragmented DNA in seminiferous tubules, as well as the number and size of vacuoles in hepatocytes, increased dose-dependently. The ovaries showed abnormal histology in the granulosa cells, which produce progesterone. There were significant differences in egg-laying rates and embryo weights between the groups. Glutathione Peroxidase 4 (GPx4) and Manganese Superoxide Dismutase (Mn-SOD), which protect the organism from oxidative damage, showed a dose-dependent decrease. Thus, it is possible neonicotinoids affect the bird's reproductive system through oxidative stress, reflecting an imbalance between the production of reactive oxygen species (ROS) and a biological system's ability to readily detoxify the reactive intermediates or easily repair the resulting damage. Responding to our study, Sado Island has since succeeded in breeding Japanese crested ibis in the wild without the use of neonicotinoids.

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

“…In red-legged partridges Alectoris rufa, reproductive effects included reduced clutch size, delayed laying dates and altered secondary sexual characteristics when exposed to imidacloprid (Lopez-Antia et al 2015a). Numbers of germ cells were reduced when Japanese quail Coturnix japonica were exposed to clothianidin (Hoshi et al 2014), while exposure of red-legged partridges to fipronil led to reductions in the levels of sex hormones, reduced egg fertility, and altered secondary sexual characteristics (Lopez-Antia et al 2015b). Imidacloprid and fipronil had deleterious effects on growth of birds, exhibited as growth retardation, reduced weight gain and lost body condition, often as a consequence of reduced food intake (Hussein et al 2014a, b;Khalil et al 2017;LopezAntia et al 2015b).…”

Immunotoxicity evaluation by subchronic oral administration of clothianidin in Sprague-Dawley rats

“…However, several studies have reported the disappearance and mass death of honeybees in Europe, as well as in America and other countries, occurring since the 1990s [18,21,65], which has raised concerns about the secondary effects of these agents on non-targeted insects. It has also recently been reported that NNs have adverse effects on vertebrates for example, on the reproductive organs in reptiles [9], birds [26,60] and mammals [67], and the emotional behavior in mice [23,24,59,68]. In order to assess the risk of NNs, therefore, there is an urgent need for definitive information about their effects on mammals.…”

A worldwide survey of neonicotinoids in honey

“…Neonicotinoids are taken up by plants and transported to all organs, including flowers, thus contaminating pollen and nectar as well as any fluid produced by the plant (3). There are increasing concerns about the impact of these systemic pesticides, not only on nontarget organismsespecially pollinators such as honey bees (4)(5)(6) and wild bees (7,8), as well as in other terrestrial and aquatic invertebrates (9, 10)-but also on vertebrates (11)(12)(13)(14), including humans (15,16). Impacts on such a broad range of organisms ultimately also affect ecosystem functioning (17).…”