Temporal trends of PBDEs and emerging flame retardants in belugas from the St. Lawrence Estuary (Canada) and comparisons with minke whales and Canadian Arctic belugas

Highlights

• Flame retardants were quantified in three whale populations from Eastern Canada.

• Greatest blubber PBDE concentrations were found in St. Lawrence Estuary belugas.

• Levels of two Dechlorane-like compounds were greatest in Canadian Arctic belugas.

• No trend was observed for PBDE concentrations in belugas between 1997–2013.

• Levels of three emerging HFRs varied significantly in belugas over this period.

Abstract

An exponential level increase of the ubiquitous halogenated flame retardant (HFR) class polybrominated diphenyl ether (PBDE) has been documented during the 1990s in endangered belugas (Delphinapterus leucas) from the St. Lawrence Estuary (SLE), Eastern Canada. The recent worldwide bans and regulations of PBDE mixtures led to their replacement by alternative HFRs (so-called emerging HFRs) that are increasingly being reported in various environmental compartments. There are, however, limited knowledge on the spatial and temporal trends of PBDEs and emerging HFRs in cetaceans, especially after restrictions on PBDE usage. The first objective of this study was to investigate the occurrence of HFRs (35 PBDE congeners and 13 emerging compounds) in the blubber of belugas and minke whales (Balænoptera acutorostrata) found dead in the Estuary or Gulf of St. Lawrence as well as belugas from Nunavik (Canadian Arctic) collected as part of the Inuit subsistence hunt. A second objective was to investigate the trends of HFR concentrations in SLE beluga males between 1997 and 2013. PBDEs were the most abundant HFRs in all three whale populations, while hexabromobenzene (HBB), Chlordene Plus (CPlus), Dechlorane Plus (DP), and Dechlorane 604 Component B (Dec-604 CB) were quantified in the majority of blubber samples. Overall, concentrations of emerging HFRs were notably greater in SLE belugas compared to the two other whale populations, with the exception of DP and Dec-604 CB that were found in greater concentrations in Canadian Arctic belugas. No significant trend in blubber PBDE concentrations was found in SLE belugas during this 17-year period. This suggests that global PBDE regulations are too recent to observe changes in PBDE concentrations in belugas from this highly HFR-exposed environment. In contrast, concentrations of HBB and CPlus in SLE belugas decreased slightly from 1997 to 2013, while DP increased up until 2000 and decreased slightly thereafter. The occurrence and temporal variations of PBDEs and their replacement products in these cetaceans warrant continuous monitoring.

Introduction

Halogenated flame retardants (HFRs) are industrial chemicals widely used in a range of consumer products (e.g., upholstered furniture, electric and electronic devices, vehicles, etc.) to comply with fire safety standards (Mack, 2004). A large number of HFRs are additives (not chemically bound to polymers), and thus can migrate out of polymeric materials to the environment. As a result, some of the most heavily used HFRs, including the polybrominated diphenyl ethers (PBDEs) used in three technical mixtures (i.e., Penta-, Octa-, and Deca-BDE), have become ubiquitous pollutants in ecosystems worldwide. This is of major environmental concern given the bioaccumulative and biomagnifying properties of PBDEs in food webs and their adverse health effects documented in a range of wildlife species (e.g., Kelly et al., 2008; Law et al., 2014; Mizukawa et al., 2009; Toms et al., 2009). Specifically, in vitro and in vivo studies have shown that exposure to PBDEs may be associated with deleterious effects on the endocrine and nervous systems, reproduction, and development in a range of species (e.g., Costa et al., 2014; Yu et al., 2015a). As a result, the Penta- and Octa-BDE technical mixtures were added to the annex A of the Stockholm Convention on Persistent Organic Pollutants (POPs) in 2009 (Stockholm Convention, 2009). More recently, Deca-BDE was regulated in Canada (Canada Gazette, 2015) and in the European Union (European Chemicals Agency, 2014), and was proposed for listing under the Stockholm Convention on POPs (Stockholm Convention, 2013). These global PBDE bans and regulations led to their replacement by alternative HFRs including pentabromoethylbenzene (PBEB), hexabromobenzene (HBB), bis(2-ethylhexyl)-tetrabromophthalate (BEHTBP), octabromo-1,3,3-trimethyl-1-phenylindan (OBIND), and decabromodiphenylethane (DBDPE). Highly halogenated norbornenes such as syn- and anti-Dechlorane Plus isomers (DP), Dechlorane-602 (Dec-602), Dec-603 and Dec-604 were also suggested as putative alternatives to Deca-BDE (Pakalin et al., 2007). Moreover, two other structurally-related Dechlorane compounds, Chlordene Plus (CPlus) and Dec-604 Component B (Dec-604 CB), have been detected in aquatic organisms (de La Torre et al., 2012, Houde et al., 2014, Shen et al., 2014). To date, no global restriction exists on the production or use of these emerging HFRs.

A number of studies have reported the environmental occurrence of PBDEs and selected emerging HFRs (e.g., HBB, PBEB, and DP) from the Laurentian Great Lakes and St. Lawrence River basin (Gentes et al., 2012, Houde et al., 2014, Su et al., 2015, Venier et al., 2015), and Arctic regions (de Wit et al., 2010, Muir and de Wit, 2010, NCP, 2013, Vorkamp and Rigét, 2014). Specifically, elevated concentrations of PBDEs were determined between 2004 and 2008 in suspended matters and sediments collected from the St. Lawrence River, with an increase in levels downstream to major urban outfalls (Pelletier and Rondeau, 2013). Elevated tissue concentrations of PBDEs and selected emerging HFRs (e.g., Dec-604 CB, Dec-602, and CPlus) were also reported in two predatory fish species (Houde et al., 2014) and two gull species occupying high trophic levels (Chen et al., 2012, Gentes et al., 2012) in the St. Lawrence River near the city of Montreal (QC, Canada). Moreover, the St. Lawrence Estuary (SLE) belugas (Delphinapterus leucas) were found to exhibit blubber concentrations of PBDEs that were among the greatest documented worldwide (males: 421 ng/g l.w.; females: 419 ng/g l.w.) (Lebeuf et al., 2014a). By comparison, notably lower PBDE concentrations (53 ng/g l.w.) were reported in the liver of Canadian Arctic belugas (McKinney et al., 2006) and blubber of a baleen whale species, the minke whale (Balænoptera acutorostrata) (range: 71–126 ng/g l.w.) from Norway, Greenland, and Iceland (Rotander et al., 2012).

Despite a nearly 40-year hunting ban, the SLE beluga population, comprised of approximately 900 individuals (Mosnier et al., 2015), is not recovering and was recently listed as endangered by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC, 2014). The lack of recovery of this population may be explained by a number of factors including climate variability and change in prey availability (Plourde et al., 2014), episodic toxic algal blooms (Scarratt et al., 2014), vessel traffic (Lesage et al., 2014, Ménard et al., 2014), and chronic exposure to environmental contaminants (e.g., PBDEs, PCBs, DDTs, polycyclic aromatic hydrocarbons, mercury, and butyltin) (Lebeuf et al., 2014b, Martineau, 2010, O'Hara et al., 2003). The concentrations of several POPs (i.e., PCBs, DDTs, and HCHs) have decreased significantly in the blubber of SLE belugas over the last 30 years (Lebeuf et al., 2007, Muir et al., 1996). In contrast, blubber PBDE concentrations in SLE belugas increased markedly from 1987 to the late 1990s, and remained stable up until 2007 (Lebeuf et al., 2014a). Similar temporal trends in PBDE concentrations were documented in Great Lakes lake trout (Salvelinus namaycush) in which an increase was observed between 1980 and 2000 (Venier et al., 2015), although followed by a decrease from 2000 up to 2009 (Crimmins et al., 2012). A limited number of studies have investigated the temporal trends of emerging HFRs in the Great Lakes. For instance, levels of several Dechlorane-related compounds were reported to slowly decrease from the 1980s to 2010 in sediments and lake trout from the Great Lakes (Ismail et al., 2009, Shen et al., 2011a). Furthermore, HBB, PBEB and DP concentrations were found to decrease steadily in Great Lakes air samples between 2005 and 2013 (Liu et al., 2016). To our knowledge, temporal trends of emerging HFRs have as yet not been investigated in aquatic species other than fish from the Great Lakes and St. Lawrence River basin - a known hotspot region for these chemicals of high environmental concern.

The objectives of the present study were two-fold. First, the blubber concentrations of HFRs (35 PBDE congeners and 13 emerging compounds) were compared between belugas found dead in the SLE and those of belugas from the eastern Canadian Arctic and minke whales (Balænoptera acutorostrata), a baleen whale occurring seasonally in the SLE and Gulf of St. Lawrence and occupying lower trophic levels than belugas (Gavrilchuk et al., 2014, Lesage et al., 2001). Second, the temporal trends of HFRs were investigated in the blubber of SLE belugas between 1997 and 2013 (pre- and post-PBDE restriction periods). Ecological factors such as trophic position (determined from stable carbon and nitrogen isotope signature), age and body length were considered in the analyses as these are known to influence the bioaccumulation dynamics of POPs in marine mammals (e.g., Hebert and Weseloh, 2006; Krahn et al., 2007; Lebeuf et al., 2014a; Reijnders et al., 2009).