High concentrations of persistent organic pollutants in adult killer whales (Orcinus orca) and a foetus stranded in Ireland
Introduction
The impact of persistent organic pollutants (POPs) in the marine environment has been of considerable concern since the 1970s as these compounds remain ubiquitous in the environment (Fiedler, 2001). Low vapour pressure, high thermal stability and the lipophilic nature of persistent organic pollutants including PCBs, PBDEs and OCs are the physico-chemical characteristics that allow them to travel and accumulate in the environment and biota respectively; even in remote areas of the globe with no previous direct anthropogenic contamination (Ikonomou et al., 2002).
PCBs have been found to accumulate in waterways, aquatic systems and adsorb onto sediment. This accumulation can be attributed to run-off from the land application of PCBs, improper disposal of electrical equipment containing PCB transfer fluids and hydraulics, as well as seepage from accidental spills and sewage (Voogt and Brinkman, 1989; Beyer and Biziuk, 2009). Brominated flame retardants, specifically poly-brominated diphenyl ethers (PBDE) and poly-brominated biphenyls (PBBs) were largely used to confer flame resistant properties in the production of textiles, plastics and electrical equipment (De Wit, 2002; Hites, 2004). Organochlorines such as dichlorodiphenylchloroethane (DDD), dichlrorodiphenylchloroethylene (DDE), dichlorodiphenyltrichlroroethane (DDT), hexachlorobenzene (HCB) as well as Dieldrin, Aldrin and Isodrin have a range of different chemical structures. The high degree of chlorination and aliphatic or aromatic cyclic structures of OCs led to their widespread use as pesticides from the 1950s–1970s (Shen and Wania, 2005), and consequently their environmental persistence and potential for long range transportation (Beyer et al., 2000).
The lipophilic nature of halogenated contaminants allows for bio-accumulation in the lipid-rich blubber of marine mammals, including killer whales, and is the cause of widespread concern not only in Europe, but on a global scale (Jepson and Law, 2016; Desforges et al., 2018). Killer whale populations in the UK and Ireland, were monitored by Beck et al. (2014) through the use of opportunistic photo-identification of individual animals over a 19 year period which suggested a slight decline of an isolated killer whale population around the Irish and British coasts had occurred. However, sparse data on this small population (n = 10) presented difficulties in defining the potential causes of this decline (Beck et al., 2014). Killer whales are apex predators, often feeding on species that occupy the highest trophic levels. This, coupled with high lipid content and a long life-span, places them at particular risk to bio-accumulation of ubiquitous POPs such as OCs, PCBs and PBDEs. These compounds pose an ongoing threat; the possible extinction of local populations has been suggested (Jepson et al., 2016; Desforges et al., 2018) as high concentrations of pollutants are consistent with reproductive and recruitment failure. A toxicity threshold of 17mg/kg in the blubber of marine animals has been suggested as leading to reproductive impacts (Kannan et al., 2000). It remains essential that concentrations of such contaminants in top predators are measured and reported. An expansion of monitoring contaminant concentrations may lead to a more holistic understanding of the impacts of such compounds and associated detriments to the species as a whole.
In an Irish context, there is limited knowledge regarding concentrations of OCs, PCBs and PBDEs in most marine mammal species including killer whales. A limited number of studies of organochlorine concentrations in some odontocete species in Irish waters have been published, such as on bottlenose dolphins (Tursiops truncatus) (Berrow et al., 2002), white-sided dolphins (Lagenorhynchus actus), (McKenzie et al., 1997), common dolphins (Delphinus delphis) and harbour porpoises (Phocoena phocoena) (Smyth et al., 2000) as well as one mysticete, the humpback whale (Megaptera novaeangliae) (Ryan et al., 2013). There is only one known sample from a killer whale from the Irish coast analysed to date in which concentrations of PCBs and a suite of organochlorines were reported (McHugh et al., 2007).
The aim of this study was to contribute to the limited knowledge of PCB, OC and PBDE contamination levels in killer whales stranded in Ireland. A pregnant female stranded in County Mayo and an adult female stranded in Waterford were analysed for a suite of 16 PCBs, and 7 PBDEs, while samples from an adult male stranded in 2017 were also analysed for a range of OCs, in addition to PCBs and PBDEs.
Section snippets
Analytical methods
All killer whale blubber samples were obtained through the Irish Whale and Dolphin Group (IWDG) Cetacean Stranding Scheme. Samples were collected from 1. Doohoma, County Mayo (54°18′35.0″N 9°58′47.8″W); 2. Roundstone, County Galway (53°23′06.2″N 10°01′37.0″W) and 3. Tramore, County Waterford (52°09′33.8″N 7°04′48.1″W) (Fig. 1, Table 1). Samples were initially stored at −20 ᵒC, before transfer to −80 ᵒC freezer storage at the Marine Institute Laboratories in Rinville Oranmore before analysis.
Quality control
Analyses of PCBs and PBDEs for both adult female killer whales as well as the foetus sample were carried out at the Marine Institute, ISO 17025 accredited for the analysis of PCBs. NIST 1947 Lake Michigan tissue was used as a certified reference material (CRM) and was analysed alongside samples. LOQs across all analytes ranged from 0.05 to 0.2 ng/g, a full list of LOQs can be found in the Supplementary Information. Procedural blanks were also run, and samples were analysed in triplicate. NIST
Results
Individual contaminant analytes were detected across all replicates from all samples. The Tramore female was found to contain a sumPCB concentration of 1.5 mg/kg on a lipid weight (lw) basis and sumBDE concentration of 0.04 mg/kg lw. The pregnant female from Doohoma was found to contain a sumPCB concentration of 49.3 mg/kg lw and a sumBDE concentration of 1.2 mg/kg. The foetus had a sumPCB concentration of 10.6 mg/kg lw and a sumBDE concentration of 0.3 mg/kg lw. SumPCB and sumBDE
Discussion
There are a wide range of factors that may have affected our results, including age, sex, and reproductive status. Diet has also been shown to be important with transient killer whales accumulating increased concentrations of contaminants due to their diet of other marine mammals in contrast to sympatric resident ecotypes which have a mainly fish-based diet (Ross et al., 2000; Krahn et al., 2007). In this study, the stranded pregnant killer whale was found to have the highest concentration of
POP concentrations
This study found sumPCB concentrations in the range of 1.5 mg/kg to 49.3 mg/kg on a lipid weight basis across all samples, values that conform to concentrations previously reported (Hayteas and Duffield, 2000; Ross et al., 2000; Kajiwara et al., 2006; Wolkers et al., 2007). To the authors’ knowledge there is only one other published account of pollutant concentrations from a killer whale sampled in Ireland; that individual, stranded at Roches Point, County Cork in 2001, was reported to have
Effects of contaminants
Ethical, legal and logistical challenges preclude controlled exposure and therefore cause-effect studies into the effects of contaminants on killer whales. However, immune, endocrine and reproductive system dysfunction has been linked to PCB contamination in a number of other odontocetes. In harbour porpoises, Jepson et al. (2005) observed a significant difference in the concentrations of PCBs between two groups of harbour porpoises. One group consisted of animals that died from acute physical
Conclusion
Concentrations of persistent organic pollutants from four killer whales stranded in Ireland were investigated. One killer whale, the Doohoma female, exceeded the suggested toxicity threshold of 17 mg/kg. The role high concentrations of persistent pollutants may have played, if any, in its possible cause of death is not known. Although this whale exceeded the toxicity threshold, the high concentration of contaminants did not appear to affect the fecundity of this animal as it was pregnant with a
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study would not have been possible without the provision of samples by the Irish Whale and Dolphin Group (http://iwdg.ie). The authors would like to thank Alessandro Pierini for his assistance in the dissection of the Doohoma mother and calf pair, and Deirdre Slevin for organising the autopsy of the individual stranded in Tramore as well as Mick O'Connell who provided information regarding the location of each carcass. GMIT's RISE scholarship program supplied funding for MS. We greately
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