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Disruption of the stress response in wastewater treatment works effluent-exposed three-spined sticklebacks persists after translocation to an unpolluted environment

Abstract

The hypothalamic–pituitary–adrenal/interrenal (HPA/I) axis plays a key role in responding to biotic and abiotic challenges in all vertebrates. Recent studies have shown that the apical response of the HPI axis to stressors in three-spined sticklebacks varies in proportion to the concentration of wastewater treatment works (WWTW) effluent to which the fish are exposed. This study was conducted to determine whether between-site variation in stress responsiveness among WWTW effluent-exposed sticklebacks is persistent or reversible. Sticklebacks from eight sites in north-west England affected by WWTW effluent and exhibiting between-population variation in HPI axis reactivity, were moved to a clean-water aquarium environment. After five months in the contaminant-free environment the responsiveness of these fish to a standardised stressor was determined, by measuring the rate of stress-induced cortisol release across the gills, and compared with the responses of fish newly sampled from the eight original capture sites. Inter-site differences in the reactivity of the HPI axis, proportional to the effluent concentration at each site, persisted among the translocated female sticklebacks for at least 5 months. In male fish however, the direct relationship between stress responsiveness and site-specific effluent was not evident 5 months post-translocation. These results support previous observations that the HPA/I axis, a non-reproductive endocrine system, is vulnerable to modulation by anthropogenic factors in fish and show for the first time that, in female fish at least, this modulation is not transient. The mechanisms underlying these observations, and the implications for the fitness and resilience of affected populations, requires investigation.

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Acknowledgments

This study was funded by the U.K. Department for Environment, Food and Rural Affairs (Defra, contract CB0472) and the U.K. Natural Environment Research Council (NERC). The authors thank Mr. J. Ben James (CEH Lancaster) for assistance with field sampling and Dr. Richard J. Williams (CEH Wallingford) for calculating the effluent concentrations at each sample site.

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Correspondence to Tom G. Pottinger.

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The authors declare that they have no conflict of interest.

Ethical approval

The confinement stress procedure to which the aquarium-held and wild-caught fish were subjected was approved by the Lancaster University Animal Welfare and Ethical Review Body and was conducted under UK Home Office licence.

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Pottinger, T.G., Matthiessen, P. Disruption of the stress response in wastewater treatment works effluent-exposed three-spined sticklebacks persists after translocation to an unpolluted environment. Ecotoxicology 25, 538–547 (2016). https://doi.org/10.1007/s10646-016-1612-3

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Keywords

  • Sewage
  • Municipal wastewater
  • Stress response
  • Cortisol