New versus legacy contaminants in Adèlie penguin (Pygoscelis adeliae): their temporal trends evaluated and compared in the climate change context

Persistent Organic Pollutants (POPs) can reach Antarctica through long-range transport mechanisms mainly via the atmosphere and oceans. The same mechanisms can transport anthropogenic mercury (Hg) to Antarctica and amplify its natural levels. Having been transported with the atmosphere, pollutants may be deposited through cold condensation or snow scavenging. Besides long-range transport, some local sources of pollution may exist including tourism, research stations and industrial fishing. Long-range transported or locally released pollutants will finally enter marine ecosystems and accumulate in the trophic webs threatening endemic species. The most studied pollutants in Antarctic biota are the legacy POPs. Among them, polychlorinated biphenyls (PCBs), hexachlorobenzene (HCB) and p,p’-dichlorodiphenyltrichloroethane (p,p’-DDT), together with its transformation products, are the most frequently studied ones in biota since the 1960s. New POPs such as polybrominated diphenyl ethers (PBDEs), and other pollutants like perfluoroalkyl substances (PFAS) have been included in monitoring studies more recently and have also been detected in endemic organisms. Hg is among the most important chemical threats for the global environment and its monitoring in Antarctic biota has been carried out since the 1970s. An international and coordinated monitoring program is lacking for the Antarctic continent and Southern Ocean, few data are available on current pollutant levels in Antarctic biota and their development over time. Monitoring chemical contamination is crucial to improve our insights into the distribution of pollutants, including data on their bioaccumulation, which can guide regulatory decisions for the protection of the environment. Moreover, temporal trend analysis is an important tool to evaluate the effectiveness of global restriction measures applied to chemicals of concern and to empirically support and validate predictive modelling studies. However, climate change has the potential to affect our ability to detect and interpret pollutant trends. Time trends could be influenced by climate-driven confounding factors such as the remobilisation from melting ice, or volatilisation from land/ice/snow/sea surface as temperatures increase. Thus, to understand how pollutant bioaccumulation dynamics will be influenced by the ongoing and expected changes, it will be important to study correlations between environmental variables and pollutant concentrations. The Ross Sea is one of the most productive areas south of the Antarctic Circle and represents an important foraging ground for many species. Moreover, its trophic web is mostly intact as demonstrated by the full suite of top and intermediate predators. Aiming to protect the unique features of this ecosystem, the Ross Sea Marine Protected Area was established in 2017. One of the key species in the Ross Sea trophic web is the Adèlie penguin (Pygoscelis adeliae), a resident mesopredator considered a good sentinel for chemical contamination. In this project, unhatched eggs of Adèlie penguin, collected from three colonies along the Ross Sea coasts, were analysed to provide updated results on legacy and new POPs (PCBs, HCB, p,p’-dichlorodiphenyldichloroethylene (p,p’-DDE) the main metabolite of DDT and PBDEs) as well as mercury, and establish a baseline for PFAS, that had not previously been reported in organisms from the selected area. Eggs collected from 1997 to 2021 were analysed to evaluate the temporal trends of PCBs, PBDEs, HCB, p,p’-DDE, and PFAS. Correlations between those compounds and climate parameters (precipitation, temperature, sea ice coverage and Antarctic Oscillation (AAO) index) were also evaluated. The PCB analysis included seven indicator PCB congeners (IUPAC nos. 28, 52, 101, 118, 138, 153 and 180) of which IUPAC nos. 28, 118, 138, 153 and 180 were detected in the eggs from the last sampling season (2021/2022). Concerning these recent eggs, average ∑PCBs ranged from 20.9 to 24.3 ng/g lipid weight (lw). Concentrations below detection limits were not included in the sum calculations. PCBs were dominated by hexa-chlorinated congeners, which agreed with previous reports. HCB and p,p’-DDE ranged between 134-166 and 181-228 ng/g lw, respectively. ∑PBDEs ranged from 0.90 to 1.18 ng/g lw and consisted of PBDE-47 (that prevailed as expected, representing 60-80% of the ∑PBDEs) and PBDE-85, while other PBDE congeners were below detection limits. ∑PFAS ranged from 1.04 to 1.53 ng/g wet weight and comprised five long-chain perfluorinated carboxylic acids (PFCAs), perfluorooctane sulfonate (PFOS), perfluorohexane sulfonate (PFHxS) and perfluorooctanoic acid (PFOA); perfluorooctane sulfonamide (PFOSA) was also detected. The PFAS profile was dominated by PFCAs as previously observed in Arctic seabirds. Mercury ranged between 0.07-0.15 mg/kg dry weight similarly to previous studies. Eggs from the three colonies belonging to the same metapopulation did not show significant differences. The levels of legacy POPs were mostly in line with past studies, but with minor variations in some cases, likely due to continued input or release from past reservoirs. PFAS were reported for the first time in penguins from the Ross Sea, highlighting their ubiquity. Same POP analyses were conducted on eggs collected between 1997 and 2021. Some PCB congeners showed a significantly decreasing trend, as expected following their phase-out several decades ago. HCB and p,p’-DDE indicated decreasing but not significant trends. The reasons for this difference are not known but might be related to the unintentional production of HCB or the ongoing use of DDT in some parts of the southern hemisphere. However, a contribution from climate-driven remobilisation mechanisms may also play a role. The time trend analysis over the period 1997-2021 confirmed the general observation of updated results on the chemical contamination status being slightly lower than or comparable to previously reported data. The only PBDE detected in >50% of samples was PBDE-47, which indicated a decreasing but not significant trend; this is in line with other studies that reported PBDEs as stable in Antarctic ecosystems likely due to their relatively recent global restriction. PFAS trends agreed with what has been previously observed in the Arctic: significantly decreasing PFOS, according to its global ban, and increasing long-chain PFCAs. The observed trends indicate the effectiveness of international regulatory measures on legacy POPs. Restriction timelines seemed to explain also the trends observed for PBDEs and PFAS both, regulated (e.g. PFOS) or not (PFCAs). Observed results confirmed the expected delayed pattern compared to Arctic trends suggesting the usefulness of considering Arctic studies results when making hypotheses on future Antarctic contamination scenarios. Some changes in accumulation patterns may be related to the changing climate conditions although current uses, unintentional production or inadequate disposal may also have affected these results. Correlations with selected climate parameters showed an inverse significant correlation between PBDE-47 levels and sampling year precipitations. While we cannot fully explain mechanisms behind these correlations, our results suggest climate change as a driver of pollutant dynamics. Further studies that include other variables connected with the ecology and biology of the species will help to increase our understanding of the influence of climate on pollutants dynamics and bioaccumulation and more generally, improved and coordinated monitoring programs will be crucial to predict future changes scenarios in Antarctica.