Chemical exposure and stress responses in UK fish - Part 2. Final report

Pottinger, Thomas G.; Matthiessen, Peter; James, J. Ben; Rhodes, Glenn; Williams, Richard J.. 2016 Chemical exposure and stress responses in UK fish - Part 2. Final report. NERC/Centre for Ecology & Hydrology, 84pp. (CEH Project no. C04734) (Unpublished)

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Executive summary: 1. The neuroendocrine stress response is a critically important adaptive mechanism in all vertebrate animals. The response is activated by events or conditions that threaten or challenge the animal (stressors). When triggered, the stress response evokes a range of physiological, endocrinological and behavioural adjustments that collectively increase the animal’s likelihood of survival. A key outcome of the response is a rapid elevation in the concentration of the steroid hormone cortisol in the blood. Measurement of stress-induced cortisol concentrations can be employed as an index of the responsiveness of the stress axis to a stressor. 2. Because the stress response is dependent upon a neuroendocrine signalling cascade it is susceptible to modulation by chemicals that mimic the hormones involved, or interfere with their synthesis or metabolism, or influence hormone-receptor interactions. Interference with the function of the stress axis will compromise the ability of the animal to mount an appropriate response to stressors and can therefore be assumed to have implications for the fitness of the animal. The term fitness in this context means the combination of all those biological processes which confer the ability to survive to reproductive age and produce appropriate numbers of normal offspring. 3. Our field surveys of three-spined stickleback populations in NW England have shown that the magnitude of the stress response, measured as both stress-induced whole-body cortisol concentrations, and the stress-induced release of cortisol to water, varies with exposure to wastewater treatment works (WWTW) effluent. We interpret this as indicating that among the range of contaminants present in WWTW effluent, one or more act to alter the responsiveness of the stress axis by directly interfering with cognitive, biosynthetic, feedback, clearance, or signalling systems. 4. The number of sites in NW England contributing to these findings strongly suggests that modulation of the responsiveness of the stress axis by exposure to WWTW effluent is a widespread phenomenon and will likely be observed at similar sites throughout the UK and elsewhere, and in species of fish in addition to three-spined stickleback. Other aquatic vertebrates are also potentially at risk. 5. At sites with no upstream WWTW input we have previously observed unexplained between-site variation in the responsiveness of the stress axis among sticklebacks. This is shown to be related to variation in a range of physico-chemical water quality determinands. A similar range of water quality determinands is also associated with variation in the stress axis at WWTW-impacted sites. These observations suggest that the modulation of the stress axis of fish is not limited to rivers with identifiable WWTW discharges but is more widespread and encompasses fish in rivers considered to be free from effluent-derived endocrine-active contaminants. 6. Variation in stress responsiveness among fish at sites unaffected by WWTW discharges and at sites downstream of WWTWs is most likely attributable to (i) the presence of unidentified contaminants that occur together with, and in proportion to, water quality indicators and have specific functional effects on the stress axis of fish, or (ii) direct effects of one or more of the core range of water quality indices themselves. For example, nitrate has been shown to disrupt steroidogenesis in fish and our results show inter alia that stress-induced cortisol release in sticklebacks downstream of WWTW discharges was positively correlated with the mean concentration of nitrate in the rivers sampled. Although this is not confirmation of a causal relationship the observation warrants further investigation. 7. Preliminary data describing variation in the abundance of human mtDNA in water samples taken from sites not receiving WWTW effluent suggests that some sites identified as being unaffected by WWTW effluent may nonetheless be exposed to sewage pollution, and presumably therefore chemical contamination associated with sewage, from sources other than documented WWTWs. 8. Variation among water quality determinands, and effluent concentration, explains a large proportion of the variation in size (mass, length) among stickleback populations exposed to WWTW effluent. Most of these relationships are negative, even though it is to be expected that the nutrient inputs from WWTWs would lead to increased growth. Size is a major determinant of fitness in fish and these findings suggest that effluent exposure reduces fitness among fish residing downstream of WWTW discharges. It remains to be established whether the negative effects on size are mediated via contaminant effects on the stress axis, or as a result of direct effects on growth-related processes, or as a reflection of energetic costs associated with adaptive responses to contaminant challenge. 9. Sticklebacks translocated from WWTW effluent-impacted sites to pristine holding conditions retained the level of stress axis reactivity associated with their sites of origin for at least 5 months post-transfer indicating that these effects are not dependent upon acute ongoing exposure to WWTW effluent, or local environmental factors. Instead, variation in stress axis reactivity is a robust trait that may reflect local adaptations at a genetic level, effects of early developmental exposure, or persistent effects on the stress axis arising from epigenetic mechanisms. 10. In summary, this project has revealed previously unsuspected, major and widespread variation in the reactivity of the stress axis of a common freshwater fish species. For fish at sites downstream of WWTW discharges this modulation of the hormonal stress response is explained in part by variation in the concentration of treated sewage effluent to which they are exposed. For fish at sites ostensibly unaffected by WWTW discharges variation in the function of the stress axis is related to variation in a range of physico-chemical indices of water quality. These observations have potentially serious implications for the overall fitness of fish in UK rivers. Furthermore, given the highly conserved nature of hormonal stress responses across all the vertebrates, there may also be implications for other species. We recommend that further work on this subject should be considered, in particular to identify the causative substance(s), and to explore the full implications for the fitness of UK fish populations.

Item Type: Publication - Report
UKCEH and CEH Sections/Science Areas: UKCEH Fellows
Rees (from October 2014)
Funders/Sponsors: Defra
Additional Keywords: stress response, cortisol, stress axis, endocrine disruption, three-spined stickleback, wastewater, sewage, WWTW
NORA Subject Terms: Ecology and Environment
Biology and Microbiology
Date made live: 22 Feb 2017 11:35 +0 (UTC)

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