Elsevier

Aquatic Toxicology

Volume 73, Issue 4, 30 July 2005, Pages 394-405
Aquatic Toxicology

Tissue levels and biomarkers of organic contaminants in feral and caged chub (Leuciscus cephalus) from rivers in the West Midlands, UK

https://doi.org/10.1016/j.aquatox.2005.05.001Get rights and content

Abstract

The Birmingham conurbation (West Midlands, UK) has traditionally been a major centre of UK industry and population and consequently has a legacy of pollution, which is reflected in the water quality of local rivers. Three of these rivers, exhibiting good, intermediate and poor overall water quality, were the subject of a study in which the effects of contamination on hepatic biomarkers and tissue contaminant loads in feral and caged chub (Leuciscus cephalus) were investigated. Muscle polychlorinated biphenyls and organochlorine pesticides (PCBs and OCPs), as well as bile pyrene and benzo[a]pyrene-like metabolite levels, were variable in both caged and feral fish, but were generally higher in tissue from the more polluted sites. OCPs were, in most cases, higher in the feral fish than in the caged fish, although the opposite was true of bile PAH metabolites, possibly due to differences in relative accumulation rates. Hepatic CYP1A activity (via ethoxyresorufin-O-deethylase (EROD) activity) in both feral and caged fish was also generally higher at the more polluted sites. EROD activity in feral and caged fish was statistically associated with polycyclic aromatic hydrocarbon (PAH) contamination and specific PCB congeners. Other biomarkers measured (reduced glutathione in liver, and serum aspartate aminotransferase) showed little consistent evidence of relationships with water quality. The assessment of these parameters during different seasons also revealed relatively little evidence of temporal variation. Overall, the caged chub appeared to reflect the pattern of general water quality more accurately than did feral fish, particularly with respect to EROD activity and to some degree bile PAH metabolites, thus supporting their use as sentinel species. However, the fact that muscle OCPs were generally higher in the feral fish suggests that the use of feral fish may be more indicative of exposure to certain classes of contaminant, and so biological monitoring programs should be designed with such considerations in mind.

Introduction

The Birmingham conurbation (West Midlands, UK) has traditionally been a major centre of industry and population, and consequently has a legacy of pollution, which is reflected in reduced water quality in many of the city's surrounding watercourses (e.g. Harkness, 1982). Of these, three local rivers, the confluent Tame, Cole and Blythe, have a history of relatively poor, intermediate and good water quality, respectively, with regard to overall contaminant levels. For example, over a number of sampling campaigns, the Blythe, Cole and Tame exhibited average total bioavailable (semi-permeable membrane device measured) water levels of PAHs of 1493, 6218 and 5825 ng/3-week exposure, PCBs of 14, 22 and 70 ng/3-week exposure, and OCPs of 137, 277 and 443 ng/3-week exposure (Garofalo et al., unpublished data). In addition, levels of heavy metals exhibited the same pattern across the three rivers (Garofalo et al., 2004). These rivers were the subject of a study in which the effects of such contamination on resident (feral) and introduced (cage-exposed) fish was investigated on a temporal basis over two consecutive years.

The river Tame, which mainly flows through an area of dense urban development and industrialization (Beavan et al., 2001), receives large amounts of industrial and urban inputs (Webster et al., 2001). In contrast, the Site of Special Scientific Interest (SSSI)-designated river Blythe (Box and Walker, 1994) has an extensively rural course, and receives relatively little detrimental chemical input. The third river, the Cole, has a predominantly urban course with relatively few industrial inputs, and exhibits overall chemical water quality intermediate to that of the other two sites, with the main deleterious inputs derived from urban runoff (Williams, 2000).

The main purpose of the current study was to determine if the measured differences in lipophilic-organic pollutants, specifically polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs), were reflected in tissue levels and specific biomarker responses in feral and caged chub (Leuciscus cephalus) at each site. This would provide an indication of the impact of this contamination on organisms present and provide information on the applicability of various strategies for assessing inland water quality. In addition, the parallel feral and caged-fish studies allowed comparison of the relative responses of the two experimental groups, thus providing information concerning possible adaptation and/or susceptibility of either group.

Chub were chosen as the species of interest due to their reported sensitivity regarding particular biomarkers (e.g. ethoxyresorufin-O-deethylase (EROD), Larno et al., 2001), their relative abundance at the sampling sites, and their availability as hatchery-reared specimens for the parallel caged-fish study. Feral chub have previously been used for inland-water determinations of a range of biomarkers across sites with different pollution statuses (e.g. Devaux et al., 1998, Larno et al., 2001, Flammarion et al., 2002, Vigano et al., 2002). Across these studies, biomarkers measured included DNA strand breaks and EROD (Devaux et al., 1998), bile PAH metabolites, DNA adducts and erythrocyte micronucleation (Vigano et al., 2002), and many of these were determined concurrently in animals from the present study (see also Winter et al., 2004). In contrast, no previous studies have been conducted on caged chub. Indeed, the number of studies in which biomarker determinations have been undertaken in caged fish of any species is relatively small (e.g. Martin and Black, 1996, Martin and Black, 1998, Van der Oost et al., 1998, Mellanen et al., 1999, Chen et al., 2001, Barra et al., 2001, de la Torre et al., 2002), with even fewer in which comparisons have been made with feral specimens of the same species.

In the present study, in addition to muscle PCBs and OCPs, a number of biomarkers related to hepatic function were measured in feral and caged chub. These were: bile PAH metabolites; cytochrome P4501A (CYP1A) levels via EROD activity; reduced glutathione (GSH); plasma aspartate aminotransferase (AST).

Section snippets

Experimental animals and sampling periods

During 2001 and 2002, three study sites on the rivers Blythe, Cole and Tame around Birmingham, West Midlands (UK) were investigated (grid references SP221822, SP202907 and SP209933, respectively). Table 1 summarises some general water quality parameters measured in the three study rivers during summer 2001 and winter 2002. All exposures/samplings of feral and caged chub (L. cephalus) were undertaken in winter/spring (between January and March) and summer/autumn (between July and October) at the

Chemical analysis of fish muscle

Total PCBs and OCPs measured in summer 2001 and winter 2002 feral and caged fish are shown in Fig. 1.

In the feral fish, total muscle PCBs (Fig. 1a) were highest in animals caught from the Tame in both seasons. Muscle OCP levels (Fig. 1b) were also highest in the Tame in summer 2001, although no difference between rivers was apparent in winter 2002. There was little evidence of consistent temporal differences in PCB levels of feral fish, although OCPs did show some temporal variation, with

Discussion

In the majority of cases, total muscle PCBs and OCPs in the feral fish reflected water levels of these contaminants, with low levels in the Blythe fish, and high levels in the Tame fish. This suggested that these animals were representatively exposed to the PCBs/OCPs present at each site, although this pattern showed some variability in fish sampled in the winter. Levels in caged fish were less consistent and no differences were detected between any of the rivers, indicating that muscle from

Acknowledgments

This paper is dedicated to the memory of our friend and colleague, Frank Verweij. This study was funded by the European Union (CityFish project, EVK1-1999-00009). The authors thank the Environment Agency (UK) for providing practical assistance and fish, and Ready Mix Concrete (UK) and Packington Estates for facilitating access to study sites.

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