Physiological and ecotoxicological interactions of copper and ocean acidification in the polychaete worms Hediste diversicolor and Alitta virens

For coastal aquatic habitats the change in seawater pH occurring as a result of ocean acidification has the potential to alter the speciation and toxicity of the many contaminants that remain in high concentrations in coastal systems. Of particular concern are metals, such as copper, whose speciation is pH sensitive within the OA range. A meta-analysis of studies to date investigating OA-contaminant interactions using marine invertebrates reveals that 72% of the 44 studies conducted have indeed focused on metals such as copper, with only a few studies looking at polycyclic aromatic hydrocarbons (PAH) and pharmaceuticals. No clear trends in the pH-effect size on contaminant toxicity for either species or contaminant group were present however, suggesting species specific physiological responses may influence this interaction as well as contaminant chemistry. A relatively understudied group were the polychaetes, a key functional group for many coastal sediments. Sediments act as a sink for contaminants where they can accumulate to high concentrations. Hence there is high potential for polychaetes to experience elevated metal exposures under reduced seawater pH as OA progresses. To address this knowledge gap, the responses of two common coastal polychaete, Alitta virens and Hediste diversicolor, were studied under three different experimental scenarios (both water-borne and sediment based) focusing on the physiological and toxicological responses under combined exposures to ocean acidification and copper. Water-borne exposures of Alitta virens to 0.25 μM copper under ambient seawater (pH 8.10) showed a significant increase in DNA damage, along with a rise in both SOD activity and lipid peroxidation. However, when exposed to copper under OA conditions (pH 7.70) there was no further increase in DNA damage and a significant decrease in SOD activity was observed alongside a fall in lipid peroxidation suggesting that OA looks to buffer the toxicity responses to this species. This is in contrast to previous studies using mussels and sea urchins, where copper toxicity responses were significantly higher when exposed under OA conditions. To assess whether local adaptations to high levels of copper contamination influences this OA-copper interaction, a population comparison using a metal resistance population of the harbour ragworm, Hediste diversicolor and a nearby non-resistant population was then conducted. Exposures were run using copper concentrations that elicit comparable toxicity responses, using 0.50 uM copper for the resistant population, compared to 0.25 uM for the non-resistant population, reflecting the two-fold differences in LC50 values for these population. These experiments reveal a significant increase by 19.70% in metabolic rate effect size (the combined stressor when compared to the control) in the resistant population compared to a decrease by 24.02% the non-resistant population, along with differences in ammonia excretion rate and the O:N ratio, thus revealing an energetic cost of this genetic resistance when faced with the combined stressors of OA and copper. These data are in line with the emerging energy limited tolerance to stressors’ hypothesis which states that tolerance to stress can be energy limited, with bioenergetics playing a central role in the tolerance to environmental stress. Finally, a more environmentally realistic exposure scenario was conducted using Alitta virens to test the influence of sediment and tidal cycles on worm acid-base and oxidative stress responses. Field measurements of sediment pH revealed that the pHNBS range over a tidal cycle varies from 6.97 to 7.87, indicating that polychaetes are already experiencing pH’s lower than the predictions for near future open oceans. In aquarium exposures, with overlying water of pHNBS 8.10, sediment pHNBS remained within the range of 7.45 to 7.31, when the overlying water was manipulated to OA conditions (pHNBS 7.70) sediment pHNBS was within the same range as the ambient treatment. The lack of change in sediment pH, despite a 0.40 unit drop in seawater pH, removed any comparative differences in physiological and toxicity end points in the worms between treatments. Tidal emersion induced a slight reduction in sediment pH, with a significant copper effect on sediment pH causing a further decrease in pH levels. Interestingly emersion resulted in a significant OA-copper interaction for coelomic fluid bicarbonate, which increased over the emersion period, however, there was no emersion driven acidosis within coelomic fluid. Overall this work further points to contaminant-OA interactions being species specific driven, in part driven by animal physiology. It also highlights the importance of environmentally relevant exposures with sediment dwelling organisms experiencing lower pH levels than the overlying seawater which could potentially affect metal speciation and could lead to OA-contaminant interactions occurring very differently in this environment. These are important considerations for ecotoxicology studies in the face of global ocean changes.

Nielson C., 2020. Physiological and ecotoxicological interactions of copper and ocean acidification in the polychaete worms Hediste diversicolor and Alitta virens. PhD thesis, University of Exeter. Thesis (restricted access).

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