Levels and endocrine disruptive effects of legacy POPs and their metabolites in long-finned pilot whales of the Faroe Islands

Abstract

The former large production and usage of persistent organic pollutants (POPs) has led to pollution of these compounds in natural environments throughout the world. Although the production and use of many POPs has been restricted for decades, pilot whales (Globicephala melas) in the North-eastern part of the Atlantic Ocean have high body concentrations of POPs, such as polychlorinated biphenyls (PCBs), organochlorinated pesticides (OCPs) and polybrominated diphenyl ethers (PBDEs). These compounds and their biological biotransformation products, i.e. metabolites, have been linked to serious health effects in mammals, including effects on the reproductive system, due to disruption of endocrine systems in the body. The aim of this thesis was to analyse levels of POPs and their metabolites in pilot whales from Faroese waters and to investigate the possible effects of the POP exposure on steroid hormones, thyroid hormones, and vitamin A, E and D, which have been suggested as sensitive biomarkers for endocrine disruptive effects. In addition, the ability of the whales to biotransform the POPs was investigated. The possible effects of the POPs on the biomarkers were studied by analysing correlative relationships between the POP concentrations and the biomarkers, and furthermore, the POP concentrations were compared to toxic reference values (TRVs) which have been suggested for toxic effects in marine mammals.
POP concentrations were analysed in liver and plasma of whales of different sexes and age classes. The results showed that PCBs and the OCP metabolite DDE were the dominating compounds in the whales. The adult females had significantly lower POP concentrations than juveniles of both sexes and adult males, most likely due to the maternal transfer of POPs to the offspring during gestation and lactation. The relative concentrations of the different POPs also differed between adult females, sub-adults and calves and indicated that highly halogenated compounds with high lipid solubility (Log Kow) and high molecular weight are less easily transferred to the offspring than the compounds with lower molecular weight that are less halogenated and less lipid soluble. Very low concentrations of metabolites, such as hydroxylated PCBs and PBDEs, were detected, and OH-CB107/OH’-CB108 was the only metabolite detected in a significant number of individuals.
The POP concentrations in the pilot whales exceeded some of the TRVs, that have been suggested for toxicological effects in marine mammals, including effects on vitamin A and E and effects on calf survival and population growth.
The biotransformation ability of the whales was studied by analysing hepatic mRNA transcripts, protein expression and/or catalytic activity of phase I and phase II enzymes. The analyses of phase I enzymes showed that the pilot whales expressed enzymes of the CYP1, 2 and 3 families and that the expressions were related to the POP exposure. Catalytic activity of the CYP1A enzymes (EROD activity) was positively correlated to POP concentrations. The most important compounds explaining the relationship between the POPs and the EROD activity were the PCBs of the metabolizing group IV, PBDEs, cis-chlordane and HCB. The mRNA expression did not correlate with the POP concentrations in the whales. Phase II biotransformation was investigated by analysing the catalytic activity of the transferases UDPGT and GST. The catalytic activity of both phase I and II enzymes were, however low, which was in accordance with the low POP metabolite concentrations found in the present pilot whales, indicating that pilot whales have a low capacity related to hepatic biotransformation of POPs.
The biomarkers for endocrine disrupting effects did generally not show high correlative relationships with the POP concentrations, but differed with age and sex of the whales, indicating that that these are important confounding factors. Nevertheless, particularly in females, positive correlations were found between a few of the more recalcitrant POPs and single steroids hormones. The thyroid hormones correlated positively with the POPs, but since the thyroid concentrations were generally higher in juveniles than in adults and most of the adult whales were females which had significantly lower POP concentrations than the juveniles, this correlation could be explained as an age effect. However, within the age groups HCB was positively correlated with thyroid hormones in both adult females and juveniles. Positive correlations between thyroid hormones and a few compounds were also detected in the calves (0-2 years of age). For vitamin A negative correlations were found between hepatic concentrations of PBDEs and hepatic retinyl palmitate concentrations in adult females. The circulating vitamin E concentration was positively correlated to the POP exposure in the juveniles, indicating a response to oxidative stress induced by the POPs. These correlations indicated that the POP compounds may have some disturbing effects on the hormone and vitamin homeostasis in the pilot whales. However, no conclusions can be made on the toxicological, organismal and ecological relevant implications of these correlations between POPs and the biomarkers.
It is concluded, that although the pilot whales were exposed to relatively high concentrations of POPs, and the concentrations exceeded some of the toxic reference levels suggested for effects on marine mammals, the POPs did not seem to have clear overall negative effects on the analysed biomarkers. This indicates that the POPs in the Faroe Island population of pilot whales may be be-low threshold levels for negative effects on steroid and thyroid hormones and vitamin A levels. This could possibly be related to the apparent low biotransformation of POPs in pilot whales and thus their low concentrations of metabolites, such as OH-PCBs and OH-PBDE, which often have been linked to the toxic effects of POPs.

Date of Award	13 Oct 2017
Original language	English
Awarding Institution	Norwegian University of Science and Technology
Supervisor	Bjørn Munro Jenssen (Supervisor), Augustine Arukwe (Supervisor), Asunción Borrell (Supervisor) & Bjarne Styrishave (Supervisor)