Exposure to PFAS is Associated with Telomere Length Dynamics and Demographic Responses of an Arctic Top Predator

Abstract

Environmental factors that can influence telomeres are diverse, but the association between telomeres and exposure to environmental contaminants is yet to be elucidated. To date, prior studies have focused on legacy persistent chlorinated pollutants (POPs), while the effects of poly- and perfluoroalkyl substances (PFAS) have been poorly documented. Here, we investigated the associations among PFAS congeners, absolute telomere length (cross-sectional approach), and telomere dynamics (rate of telomere length change over time, longitudinal approach) in one of the most contaminated arctic top predators, the glaucous gull Larus hyperboreus from Svalbard. We further estimated the effect of PFAS on apparent survival rates and re-sighting probabilities using a 10-year capture/recapture dataset (2010–2019). We found that birds exposed to higher concentrations of perfluorononadecanoate (PFNA) (median of 1565 pg/mL of ww in males and 1370 pg/mL of ww in females) and perfluorotetradecanoate (PFTeDA) (median of 370 pg/mL of ww in males and 210 pg/mL of ww in females) showed the slowest rate of telomere shortening. We also found that high blood concentrations of perfluorooctanoate (PFOA) (median of 120 pg/mL of ww in males and 150 pg/mL of ww in females) and perfluorohexanesulfonate (PFHxS) (median of 495 pg/mL of ww in males and 395 pg/mL of ww in females) were positively associated with higher re-sighting probabilities and apparent survival in males but not in females. Our work is the first to report an association between single PFAS compounds and telomeres, and the first to link PFAS exposure with survival probabilities, suggesting that the effect of PFAS exposure might be more tied to the type of compound rather than the total concentration of PFAS.

The fate of poly- and perfluoroalkyl substances in a marine food web influenced by land-based sources in the Norwegian Arctic

“…This is in agreement with recent studies conducted on PFASs in plasma samples of glaucous gull from Svalbard. 86,89 This observation has also been made for other Arctic biota, including sh, birds and mammals. 90 Long-range transport and degradation of FTOHs is assumed as a source for the observed long-chain PFCAs in arctic animals.…”

“…This agrees with recent studies where sex-related differences in PFAS concentrations were reported. 86,89 Since the gulls were sampled prior to breeding, it is likely that they have been exposed to and accumulated PFAS when feeding in their wintering grounds. Thus, the PFAS body burdens of the bird constitutes of a mixture of PFAS compounds that have accumulated during feeding in their unknown wintering grounds, and in the Adventord following their return to Svalbard.…”

Development in the European flounder (Platichthys flesus) of a q-PCR assay for the measurement of telomere length, a potential biomarker of pollutant effects for biomonitoring studies

“…In chicks of white-tailed eagles Haliaeetus 621 albicilla, no relationship between the concentrations of organohalogenated compounds (PCBs, DDT, 622 HCH, HCB: hexachlorobenzene) and TL was observed, despite significant changes in the antioxidant 623 enzyme superoxide dismutase, plasma non-enzymatic antioxidant capacity and oxidative damage to 624 plasma proteins (Sletten et al, 2016, Costantini et al, 2019. In contrast, in the adult glaucous gull 625 Larus hyperboreus, some single PFAS compounds are positively correlated with the slowest rate of 626 telomere shortening (Sebastiano et al, 2020). Similar to humans, the, contaminant effect on telomere 627 dynamics in birds seems to vary according to the nature of the contaminant and the species.…”

Telomeres and anthropogenic disturbances in wildlife: A systematic review and meta‐analysis

“…So far, we lack key information on the causal relationship between specific disturbances and the organismal response in terms of telomeres. Moreover, we are in need of studies exploring the link between telomere length and individuals' fitness or performance in anthropogenically influenced scenarios, which has been done only recently in a handful of studies and with a mixed results (Kirby et al, 2019;Louzon et al, 2020;Salmón et al, 2017;Scholten et al, 2020;Sebastiano et al, 2020). Both are critical aspects for the broad implementation of telomeres in the estimation of ecological risk (Calow & Forbes, 1998;Forbes et al, 2006;Timbrell, 1998).…”