The effects of 4-nonylphenol and atrazine on Atlantic salmon (Salmo salar L) smolts

Abstract

Exposure of Atlantic salmon (Salmo salar L.) smolts in freshwater to environmental levels of the oestrogenic chemical 4-nonylphenol (4-NP) (concentrations 5–20 μl l⁻¹) during the peak migration period had no significant effect on gill Na⁺K⁺ATPase activity, plasma vitellogenin (VTG) levels or hypoosmoregulatory performance as indicated by survival in sea water. However, where smolts were exposed to mixtures of 4-NP and the pesticide atrazine at concentrations of 5.0/1.0 and 10.0/2.0 μg l⁻¹, respectively, there were significant differences in the gill Na⁺K⁺ATPase activity, plasma Cl⁻ and Na⁺ and increased mortalities when transferred to seawater. Smolts retained for a short period in an estuary with high levels of oestrogenic contamination showed no significant differences in gill Na⁺K⁺ATPase activity, plasma vitellogenin (VTG) levels or hypoosmoregulatory performance compared to fish maintained in an adjacent uncontaminated estuary. The results of the study are discussed in relation to the effects of environmental levels of oestrogenic contaminants on smoltification and migration in wild salmon.

Introduction

There is now a great deal of evidence that a suite of chemicals can significantly affect the endocrine systems of aquatic organisms. These so-called endocrine disrupting chemicals (EDCs) include natural and synthetic oestrogens (e.g. oestradiol and ethinyl oestradiol, respectively) man-made xenoestrogens (e.g. 4-nonylphenol) and a number of pesticides Sumpter, 1999, Moore and Waring, 1998, Moore and Waring, 2000. The majority of recent research has concentrated on the impact of xenoestrogens on the reproductive endocrine systems of fish Bortone and Davis, 1994, Jobling et al., 1998 where plasma vitellogenin has been used a biomarker for exposure of male fish to oestrogens (Sumpter and Jobling, 1995). However, less emphasis has been placed on the impact of EDCs on other endocrine systems in fish such those controlling the parr–smolt transformation in salmonids (Boeuf, 1993).

During smoltification, there is evidence that certain hormones positively regulate some aspects of the transformation. These include thyroid hormones, growth hormone (GH), cortisol and insulin-like growth factor-I Hoar, 1988, Sakamoto et al., 1995. Other hormones such as prolactin negatively regulate smoltification by counteracting the SW-adaptive effect of GH and cortisol (Madsen and Bern, 1992). The sex steroids testosterone and 17β-estradiol (E₂) have also been shown to have an antagonistic effect on smoltification. Generally, circulating levels of sex steroids are low in juvenile salmonids but where they are elevated such as in mature male parr this may subsequently inhibit osmoregulatory and other physiological aspects involved in smoltification Langdon and Thorpe, 1985, Lundquist et al., 1990, Saunders et al., 1994.

Exposure of wild juvenile salmonids to xenoestrogens and pesticides during the parr–smolt transformation could therefore have an antagonistic effect on smolt physiology and compromise the ability of the fish to osmoregulate and survive in the marine environment. Recently, Madsen et al. (1997) demonstrated that injections of E₂ and 4-nonylphenol significantly inhibited the development of smolt characteristics as judged by a significant reduction in gill Na⁺K⁺ATPase activity and poorer hypoosmoregulatory performance of the treated fish.

The present study investigated the effects of environmental concentrations of two EDCs on some aspects of smoltification in the Atlantic salmon. Firstly, smolts were exposed in freshwater to low levels of 4-nonylphenol (4-NP) and the effects on gill Na⁺K⁺ATPase activity, plasma vitellogenin (VTG), ions and seawater survival measured. 4-NP is an alkylphenol, which is a degradation product of alkylphenol polyethoxylates used widely as non-ionic surfactants. Secondly, smolts were again exposed in freshwater to combinations of 4-nonylphenol and environmental levels of the pesticide atrazine, which has previously been demonstrated to effect smolt physiology and hypoosmoregulatory performance (Waring and Moore, 1996). Thirdly, a field based study was carried out in a river estuary contaminated with oestrogenic compounds to determine any possible effects on aspects of smoltification in migratory fish.