Disruptive effects of persistent organohalogen contaminants on thyroid function in white whales (Delphinapterus leucas) from Svalbard

Abstract

We analysed levels of 56 organohalogen contaminants (OHCs) including brominated flame retardants, polychlorinated biphenyls (PCBs), and organochlorine pesticides in the blubber of white (beluga) whales (Delphinapterus leucas) from Svalbard, Norway (N = 12; 6 adults [5 males and 1 female] and 6 subadults [4 males and 2 females]) collected in 1996–2001. We also measured circulating levels of thyroid hormones (THs) and thyroid stimulating hormone (TSH) in the whales. The results confirm that OHC levels in these white whales are among the highest levels recorded in wildlife from Svalbard, and at the high end of the range when compared to white whales from the North American Arctic. A projection to latent structure (PLS) model (subadults and adult males grouped together) revealed that known or suspected thyroid disruptive contaminants (polybrominated diphenylether [PBDE]-28, -47, -99, -100, and -154, hexachlorobenzene [HCB], and PCB-105) were negatively correlated with circulating levels of total thyroxin (TT4), free T4 (FT4) and free triiodothyronine (FT3). Most of these negative relationships were also confirmed using partial correlations controlling for length (and thus age) of the whales. The positive correlations of TT4, FT4 and FT3 with hexabromocyclododecane (HBCD), α-hexachlorocyclohexane (α-HCH), chlorinated bornanes CHB-40 and CHB-62 revealed by the PLS model were not confirmed by partial correlations. TH levels in the present study appeared to be somewhat lower than levels measured in beluga whales from the Canadian Arctic. However, we were not able to determine if this was caused by different levels of OHCs, or differences in biological factors (e.g. age, sex, moulting status, and season) and analytical methods between the studies. Although the sample sizes were low and statistical models cannot depict the biological cause–effect relationships, this study suggests negative influences of specific OHCs, particularly PBDEs, on thyroid hormone levels in white whales. The impact this might have on individual and population health is unknown.

Introduction

The complex mixture of anthropogenic, long-range transported organohalogen contaminants (OHCs) that accumulates in arctic wildlife might disrupt endocrine systems and thus potentially affect development, behaviour, fertility and survival (Rolland, 2000, AMAP, 2002, Letcher et al., 2010). This is a cause for concern for arctic top-predators, especially in areas with high contaminant loads, such as the European Arctic (Letcher et al., 2010). Endocrine disrupting chemicals might also reduce an individual's ability to adapt to the ongoing climate-related changes in the Arctic (Jenssen, 2006).

One important target of endocrine disruptive chemicals is the thyroid hormone system. In vertebrates, triiodothyronine (T3) and tetraiodothyronine (thyroxine, T4) are produced by the thyroid gland. Production and secretion of these thyroid hormones (THs) are induced by thyroid stimulating hormone (TSH), which is released from the pituitary gland (McNabb, 1992). T4 is produced by the thyroid gland in much larger quantities than T3. Deiodination of T4 in extra-thyroidal tissues is the main source of the biological more active hormone, T3. Circulating T3 and T4 are responsible for negative feedback (inhibition) on pituitary release of TSH (McNabb, 1992, Hadley, 1996, Zoeller et al., 2007). THs are involved in regulation of temperature, metabolism, reproduction and growth, and are especially important for the growth and development of the nervous system in foetuses, neonates and juveniles (McNabb, 1992). Neurodevelopmental effects (e.g. cognitive dysfunctions, behaviour changes, and reduced motor skills) have been observed in human and rodent offspring exposed to OHCs in utero and postnatally through lactation. These effects are thought to be mediated via the capacity of these contaminants to disrupt TH homeostasis in sensitive periods of TH-dependent brain development (Porterfield, 2000, Howdeshell, 2002, Branchi et al., 2003, Zoeller and Crofton, 2005, Nakajima et al., 2006, Zoeller et al., 2007). Neurodevelopmental deficits in young mammals can reduce their ability to learn (and thus affect their ability to find and hunt prey), change behaviour (e.g. mating) and ultimately affect reproduction and survival. Furthermore, disturbances of the TH system can also reduce an individual's ability to thermoregulate and to adjust metabolic rate in relation to external factors such as temperature, ice-cover, food availability (fasting), migratory needs or other shifts in energy requirements. Thyroid disruptive effects of polychlorinated biphenyls (PCBs) and other OHCs have been documented in experimental in vivo and in vitro studies, and similar findings have been reported in studies of Arctic wildlife and human populations (e.g. Braathen et al., 2004, Verreault et al., 2007, Dallaire et al., 2009, Villanger et al., 2011).

White whales (beluga whales, Delphinapterus leucas) are long-lived, arctic predators that feed high in the marine food chain. They have poor capacity to metabolise and excrete OHCs (Norstrom et al., 1992, Letcher et al., 2000), and are known to accumulate high levels of these contaminants in their large blubber lipid-reservoirs (Andersen et al., 2001, Andersen et al., 2006, Wolkers et al., 2004, Wolkers et al., 2006, Letcher et al., 2010). Some of the most conspicuous effects associated with OHCs in wildlife have been reported for beluga whales from the southern end of this species' range in the St Lawrence River Estuary (Canada). Here, the high levels of OHCs and other contaminants (e.g. polyaromatic hydrocarbons) in past decades were coincident with high incidences of neoplasia and other lesions, immune dysfunction, abnormal sexual development, reduced reproduction and high mortality rates of this population (De Guise et al., 1995, Martineau et al., 2003). However, differences in exposure patterns and levels complicate extrapolation from previously reported effects in stranded St Lawrence beluga whales to potential negative effects on health in arctic populations (Letcher et al., 2010). But the past findings from the St Lawrence population demonstrate this species' susceptibility to effects of chemical contamination in the marine ecosystem that they inhabit.

Physiological studies of white whale stocks from the Canadian Arctic have reported some unique features in the TH system of this species, such as an unusually large thyroid gland, and high levels of T4 and reverse T3 (rT3) (St Aubin and Geraci, 1988, St Aubin and Geraci, 1989, St Aubin, 2001). Though many unanswered questions regarding the function and regulation of the thyroid system in white whales remain, studies indicate that THs are important in this species. These hormones are thought to play a critical role in their opportunistic life-strategies (St Aubin and Geraci, 1988, St Aubin and Geraci, 1989, St Aubin, 2001), and thus their adaptability to environmental changes, such as arctic climate changes. White whales are considered vulnerable to climate changes because of the predicted changes in their ice-habitats and they have repeatedly been recommended as a key species for monitoring change in the arctic environment (IWC, 1997, Kovacs and Lydersen, 2008, Kovacs et al., 2010).

Previous investigations of white whales from Svalbard show that OHC levels are relatively high in comparison with other marine mammals, such as polar bears (Ursus maritimus) and seals (Andersen et al., 2001, Andersen et al., 2006, Wolkers et al., 2004, Wolkers et al., 2006). OHC-associated responses of THs and other potential detrimental health effects have been reported in polar bears from Svalbard and East Greenland (Skaare et al., 2001, Braathen et al., 2004, Letcher et al., 2010, Sonne, 2010, Villanger et al., 2011). But to date no studies have investigated the possible effects of OHCs on TH homeostasis in beluga whales from the European Arctic, or in populations elsewhere. A study of beluga whales from the St Lawrence Estuary and in Hudson Bay documented hyperplasia of the thyroid gland, but it was uncertain if this was linked to OHC exposure (Mikaelian et al., 2003). Hence, the objectives of this study were to: a) measure levels of OHCs accumulated in adipose (blubber) tissue of white whales from Svalbard, b) determine circulating concentrations of THs and TSH in the same whales, and c) assess the multivariate relationships between OHC concentrations and levels of THs and TSH.