Maternal antioxidant provisioning mitigates pollutant-induced oxidative damage in embryos of the temperate sea urchin Evechinus chloroticus.

One mechanism of pollution resistance in marine populations is through transgenerational plasticity, whereby offspring capacity to resist pollution reflects parental exposure history. Our study aimed to establish correlations between oxidative stress biomarkers and key reproductive fitness parameters in the temperate sea urchin Evechinus chloroticus following exposure to dietary polycyclic aromatic hydrocarbons (PAHs). PAH-exposed adults exhibited total gonad tissue concentrations of PAHs in excess of 4 and 5 times baseline levels, for females and males respectively. Antioxidant enzymes were upregulated and oxidative lipid and protein damage to gonad tissues occurred. In addition, early stage offspring reflected maternal antioxidant status, with progeny derived from exposed females demonstrating significantly higher baselines than those derived from control females. Maternal exposure history enhanced the capacity of embryos to minimise oxidative damage to lipids and proteins following exposure to additional PAHs, but provided less of an advantage in protection against oxidative DNA damage. Abnormal embryonic development was largely independent of oxidative damage, remaining high in all embryo populations regardless of parental PAH-history. Overall, results document evidence for maternal transfer of antioxidant potential in E. chloroticus, but imply that a short-term inherited resilience against oxidative stress may not necessarily translate to a fitness or survival gain.

Dietary pollutants induce oxidative stress, altering maternal antioxidant provisioning and reproductive output in the temperate sea urchin Evechinus chloroticus.

Evidence is growing to suggest that the capacity to withstand oxidative stress may play an important role in shaping life-history trade-offs, although little is known on the relationship in broadcast spawning marine invertebrates. In this group, variation in gamete quantity and quality are important drivers of offspring survival and successful recruitment. Therefore the provisioning of eggs with antioxidants may be an important driver of life history strategies because they play a critical role in preventing damage from reactive oxygen species to macromolecules. In this study, a suite of oxidative stress biomarkers was measured in the gonads and eggs of the sea urchin Evechinus chloroticus exposed to polycyclic aromatic hydrocarbons (PAHs). Links between oxidative stress markers and core components of fitness including fecundity, gamete quality and maternal transfer of antioxidants were assessed. Experimental induction of oxidative stress was achieved via exposure to a mix of four PAHs over a 21-day period. In PAH exposed individuals, we observed a significant upregulation of the antioxidant defence and detoxification enzymes SOD, CAT, GR, GPx and GST, as well as a greater pool of the non-enzymatic antioxidant glutathione in gonad tissue and eggs. In contrast, glutathione redox status was not affected by PAH exposure, with the percentage of reduced glutathione remaining at approximately 80% in both gonad tissue and released eggs. PAH-exposed adults experienced greater than three- and five-fold increases in oxidative protein and lipid damage, respectively, in gonad tissue. In contrast, eggs maintained low levels of damage, not differing from baseline levels found in eggs released from PAH-naïve mothers. PAH exposure also resulted in a 2-fold reduction in fecundity of reproductively mature females but no significant alteration to egg diameter. Although PAH-exposed females released fewer eggs, successful fertilisation of those eggs was slightly enhanced with average rates ranging from 90-99% in comparison to 76-90% in control eggs. Early-stage offspring reflected maternal antioxidant status with populations derived from PAH-exposed mothers demonstrating significantly higher antioxidant levels than those derived from PAH-naïve mothers. This maternally inherited protection enhanced the capacity of embryos to minimise oxidative damage to lipids and proteins during early development but, despite this, did not reduce the proportion of morphological abnormalities in the population. Overall, these findings indicate that when faced with short-term contaminant stress E. chloroticus has the capacity to trade high reproductive output during a spawning event for a greater antioxidant investment in eggs. However, this production of potentially more resilient offspring did not translate to a fitness gain, at least for the early larval stages in the present experimental conditions.

Pollutant resilience in embryos of the Antarctic sea urchin Sterechinus neumayeri reflects maternal antioxidant status.

Legacy pollutants, including polycyclic aromatic hydrocarbons (PAHs) and metals, can occur in high concentrations in some Antarctic marine environments, particularly near scientific research stations. Oxidative stress is an important unifying feature underlying the toxicity of many chemical contaminants to aquatic organisms. However, the potential impacts of pollutants on the oxidative physiology of Antarctic marine invertebrates are not well documented. Sterechinus neumayeri is a common animal in the shallow subtidal benthos surrounding Antarctica, and is considered an important keystone species. The aim of the present study was to collect baseline oxidative biomarker data for S. neumayeri and to investigate the impacts of field exposure to chemical contaminants on gamete health and parent-to-offspring transfer of oxidative stress resilience. We analysed antioxidant enzyme activities, levels of the molecular antioxidant glutathione, protein carbonylation, lipid peroxidation and levels of 8-OHdG as oxidative stress biomarkers in S. neumayeri from a contaminant-impacted site near McMurdo Station and a relatively pristine site at Cape Evans. Biomarkers were analysed in adult gamete tissue and in early stage embryos exposed to AN8 fuel oil. PAHs were quantified as a proxy for contamination and were found to be elevated in urchins from the contaminated site (up to 231.67ng/g DW). These contaminant-experienced adult urchins produced eggs with greater levels of a broad suite of antioxidants, particularly superoxide dismutase, catalase and glyoxalase-I, than those from Cape Evans. In addition, embryos that were derived from contaminant-experienced mothers were endowed with higher baseline levels of antioxidants, which conferred an enhanced capacity to minimize oxidative damage to lipids, proteins and DNA when exposed to AN8 fuel. This pattern was strongest following exposure to 900ppm AN8, where lipid and protein damage was 5-7 times greater than baseline levels in contaminant-naïve female embryos in comparison to 3-4 times greater in contaminant-experienced female embryos. Despite this inherited resilience against oxidative stress, abnormal development was as high in these embryos when exposed to AN8 as in those derived from contaminant-naïve mothers (up to 80% abnormality), implying the conferred advantage may not translate to a fitness or survival gain, at least up to the blastulae stage. Our findings document the first evidence for parent-to-offspring transfer of oxidative stress resilience in an Antarctic marine invertebrate.

Sea ice protects the embryos of the Antarctic sea urchin Sterechinus neumayeri from oxidative damage due to naturally enhanced levels of UV-B radiation.

The 'ozone hole' has caused an increase in ultraviolet B radiation (UV-B, 280-320 nm) penetrating Antarctic coastal marine ecosystems, however the direct effect of this enhanced UV-B on pelagic organisms remains unclear. Oxidative stress, the in vivo production of reactive oxygen species to levels high enough to overcome anti-oxidant defences, is a key outcome of exposure to solar radiation, yet to date few studies have examined this physiological response in Antarctic marine species in situ or in direct relation to the ozone hole. To assess the biological effects of UV-B, in situ experiments were conducted at Cape Armitage in McMurdo Sound, Antarctica (77.06 degrees S, 164.42 degrees E) on the common Antarctic sea urchin Sterechinus neumayeri Meissner (Echinoidea) over two consecutive 4-day periods in the spring of 2008 (26-30 October and 1-5 November). The presence of the ozone hole, and a corresponding increase in UV-B exposure, resulted in unequivocal increases in oxidative damage to lipids and proteins, and developmental abnormality in embryos of S. neumayeri growing in open waters. Results also indicate that embryos have only a limited capacity to increase the activities of protective antioxidant enzymes, but not to levels sufficient to prevent severe oxidative damage from occurring. Importantly, results show that the effect of the ozone hole is largely mitigated by sea ice coverage. The present findings suggest that the coincidence of reduced stratospheric ozone and a reduction in sea ice coverage may produce a situation in which significant damage to Antarctic marine ecosystems may occur.