Impacts of ionising radiation on sperm quality, DNA integrity and post-fertilisation development in marine and freshwater crustaceans

Neil Fuller,Jim T Smith,Alex T Ford

doi:10.1016/j.ecoenv.2019.109764

Neil Fuller, Jim T Smith + Show 1 more

Open Access

https://doi.org/10.1016/j.ecoenv.2019.109764

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Abstract

Crustaceans have been designated as internationally important model organisms in the development of environmental radioprotection measures. Despite the known sensitivity of sperm to ionizing radiation, the impacts of chronic radiation exposure on male fertility in crustaceans have not been studied. For the first time, the present study aimed to assess the impacts of chronic radiation exposure on male fertility, sperm DNA damage and concomitant impacts on breeding in two amphipod crustaceans. Echinogammarus marinus and Gammarus pulex (male fertility only) were exposed to phosphorus-32 at dose rates of 0, 0.1, 1 and 10 mGy/d and sperm parameters, DNA damage and knock-on impacts on breeding were assessed. Sperm quality parameters and DNA damage were assessed using a fluorescent staining method and single cell gel electrophoresis respectively. Concomitant effects of male exposure to radiation on fecundity were determined by pairing phosphorus-32 exposed males to unexposed sexually mature females. In E. marinus, a statistically significant reduction of 9 and 11% in the quality of sperm was recorded at dose rates of 1 and 10 mGy/d respectively, with no significant effects recorded on sperm counts. Conversely in the freshwater G. pulex, no significant impact of radiation on sperm quantity or quality was recorded. For E. marinus, a statistically significant increase in DNA damage was recorded at doses of 10 mGy/d. Reduced fecundity and an increase in the frequency of abnormal embryos was recorded in female E. marinus breeding with males exposed to radiation. These findings suggest sperm quality may be a sensitive indicator of radiation exposure in invertebrates with potential impacts on the unexposed embryo, though unclear dose-response and differences between two closely related species necessitate further study before robust conclusions can be drawn.

Highlights

Radioactive substances are discharged in to the environment both as part of the normal operation of nuclear facilities and accidental releases such as those at the Chernobyl and Fukushima Dai-ichi nuclear power plants (NPPs)
Values were close to the desired concentrations of 62.9, 6.29 and 0.629 Bq/ml required to achieve target dose rates based on a preliminary study of 32P uptake in Echinogammarus marinus
The finding of no significant effect of radiation exposure on moulting in E. marinus and G. pulex is consistent with the work of Hoppenheit (1973) and Hoppenheit and Woodhead (1980), who recorded no significant effect of high doses of X-rays and Americium-241 (241Am) on moulting in the brackish water amphipod, Gammarus duebeni

Summary

Introduction

Radioactive substances are discharged in to the environment both as part of the normal operation of nuclear facilities and accidental releases such as those at the Chernobyl and Fukushima Dai-ichi nuclear power plants (NPPs). Studies have demonstrated the sensitivity of sperm to radiation in a range of organisms including birds (Møller et al, 2008), fish (Knowles, 1999) and rodents (Liu et al, 2006). Møller et al (2008), demonstrated perturbations to sperm behaviour and morphology in barn swallows inhabiting areas of Chernobyl with mean dose rates of 3.74 μGy/hr, which is lower than environmental dose rates in natural high-background areas (e.g. Kerala, India, maximum dose rates of 7.99 μGy/hr (Nair et al, 1999)). Recent studies have focused on the impacts of Fukushima-derived radiation on male fertility in rodents (Okano et al, 2016) and bulls (Yamashiro et al, 2013), finding no significant effect of radiation exposure (maximum mean ambient dose rates of 13.9 μSv/hr for rodents and mean total dose of 8 mGy for bulls) on sperm morphology and Ecotoxicology and Environmental Safety 186 (2019) 109764 spermatogenesis respectively. Typical endpoints in invertebrate radioecology are biased towards female reproductive success such as egg production, time of hatching and egg mass (Fuller et al, 2015)

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