Marine Pollution Bulletin xxx (xxxx) xxxx Contents lists available at ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul High concentrations of persistent organic pollutants in adult killer whales (Orcinus orca) and a foetus stranded in Ireland ∗ Moira Schlingermanna, , Simon Berrowa,b, Darren Craigb, Brendan McHughc, Michael Marrinana, Joanne O'Briena,b, Ian O'Connora, Conor Ryana, Engelberth Mudzatsia, Philip Whitea a Marine and Freshwater Research Centre, Galway-Mayo Institute of Technology, Dublin Road, Galway, Ireland b Irish Whale and Dolphin Group, Merchants Quay, Kilrush, Co Clare, Ireland c Marine Institute, Rinvill, Oranmore, Co Galway, Ireland ARTICLE INFO ABSTRACT Keywords: Bio-accumulation of persistent organic pollutants including polychlorinated biphenyls (PCBs), brominated flame Killer whale retardants and organochlorine pesticides continue to be of major concern for marine apex predators such as Ireland killer whales. The concentrations of 16 polychlorinated biphenyls, 7 poly-brominated diphenyl ethers (PBDEs), 1 PCB poly-brominated biphenyl (PBB) and a range of 19 organochlorine compounds (OCs) was investigated in blubber PBDE samples from a mother-foetus pair, an adult female and an adult male killer whale stranded in Ireland between Organochlorine 2010 and 2017. Concentrations ranged from 1.5 mg/kg to 49.3 mg/kg lipid weight and 0.04–1.2 mg/kg lipid weight for Σ16PCBs and Σ7PBDEs respectively. Concentrations of organochlorine compounds were also in- vestigated in the male killer whale; a Σ19OC concentration of 49.4 mg/kg lipid weight was recorded. This study shows high levels of persistent organic pollutants occur in this species of whales stranded in Ireland. 1. Introduction hexachlorobenzene (HCB) as well as Dieldrin, Aldrin and Isodrin have a range of different chemical structures. The high degree of chlorination and The impact of persistent organic pollutants (POPs) in the marine aliphatic or aromatic cyclic structures of OCs led to their widespread use as environment has been of considerable concern since the 1970s as these pesticides from the 1950s–1970s (Shen and Wania, 2005), and conse- compounds remain ubiquitous in the environment (Fiedler, 2001). Low quently their environmental persistence and potential for long range vapour pressure, high thermal stability and the lipophilic nature of transportation (Beyer et al., 2000). persistent organic pollutants including PCBs, PBDEs and OCs are the The lipophilic nature of halogenated contaminants allows for bio- physico-chemical characteristics that allow them to travel and accu- accumulation in the lipid-rich blubber of marine mammals, including mulate in the environment and biota respectively; even in remote areas killer whales, and is the cause of widespread concern not only in of the globe with no previous direct anthropogenic contamination Europe, but on a global scale (Jepson and Law, 2016; Desforges et al., (Ikonomou et al., 2002). 2018). Killer whale populations in the UK and Ireland, were monitored PCBs have been found to accumulate in waterways, aquatic systems by Beck et al. (2014) through the use of opportunistic photo-identifi- and adsorb onto sediment. This accumulation can be attributed to run-off cation of individual animals over a 19 year period which suggested a from the land application of PCBs, improper disposal of electrical equip- slight decline of an isolated killer whale population around the Irish ment containing PCB transfer fluids and hydraulics, as well as seepage and British coasts had occurred. However, sparse data on this small from accidental spills and sewage (Voogt and Brinkman, 1989; Beyer and population (n = 10) presented difficulties in defining the potential Biziuk, 2009). Brominated flame retardants, specifically poly-brominated causes of this decline (Beck et al., 2014). Killer whales are apex pre- diphenyl ethers (PBDE) and poly-brominated biphenyls (PBBs) were lar- dators, often feeding on species that occupy the highest trophic levels. gely used to confer flame resistant properties in the production of textiles, This, coupled with high lipid content and a long life-span, places them plastics and electrical equipment (De Wit, 2002; Hites, 2004). Organo- at particular risk to bio-accumulation of ubiquitous POPs such as OCs, chlorines such as dichlorodiphenylchloroethane (DDD), dichlror- PCBs and PBDEs. These compounds pose an ongoing threat; the possible odiphenylchloroethylene (DDE), dichlorodiphenyltrichlroroethane (DDT), extinction of local populations has been suggested (Jepson et al., 2016; ∗ Corresponding author. E-mail address: [email protected] (M. Schlingermann). https://doi.org/10.1016/j.marpolbul.2019.110699 Received 10 June 2019; Received in revised form 22 October 2019; Accepted 29 October 2019 0025-326X/ © 2019 Published by Elsevier Ltd. Please cite this article as: Moira Schlingermann, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110699 M. Schlingermann, et al. Marine Pollution Bulletin xxx (xxxx) xxxx Desforges et al., 2018) as high concentrations of pollutants are con- sistent 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 es- sential 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 im- pacts of such compounds and associated detriments to the species as a whole. In an Irish context, there is limited knowledge regarding con- centrations 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 por- poises (Phocoena phocoena)(Smyth et al., 2000) as well as one mysti- cete, 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 orga- nochlorines 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 fe- male 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. Fig. 1. Map showing sites of stranding and whale blubber sampling. 2. Analytical methods ( ± 0.1 g) deactivated alumina [5% w/w] and 1.5 g ( ± 0.1 g) deacti- All killer whale blubber samples were obtained through the Irish vated silica [5% w/w]. Whale and Dolphin Group (IWDG) Cetacean Stranding Scheme. An Agilent GC-MS equipped with a 60 m HT8 capillary column was Samples were collected from 1. Doohoma, County Mayo (54°18′35.0″N used for the analysis. Oven temperature programming was employed to 9°58′47.8″W); 2. Roundstone, County Galway (53°23′06.2″N achieve resolution of analyte peaks. A concentrated stock was run using 10°01′37.0″W) and 3. Tramore, County Waterford (52°09′33.8″N Scan mode for the identification of contaminant ions and fragmentation ᵒ 7°04′48.1″W) (Fig. 1, Table 1). Samples were initially stored at −20 C, spectra. Single ion monitoring (SIM) mode was used for the quantifi- ᵒ before transfer to −80 C freezer storage at the Marine Institute La- cation of PCB, PBDE and OC analytes. Electron ionization methods were boratories in Rinville Oranmore before analysis. Samples from killer employed in negative ion mode. SIM parameters used for the analysis whales stranded in Doohoma and Tramore, both adult females and the can be found in the Supplementary Information. Analysis of all samples foetus, were analysed for a suite of 16 PCBs (Ballschmitter and Zell and standards in SIM mode allowed for increased specificity and sen- notation used: Congeners 18, 31, 28, 52, 44, 101, 149, 118, 153, 105, sitivity. 138, 156, 180, 170, 194, 209) and 7 PBDEs (Congeners 28, 47, 100, 99, 154, 153, 183). The sample from Roundstone was analysed for the same 16 PCBs, 4 PBDEs (Congeners 47, 100, 99, 153), PBB 153 as well as 19 3. Quality control OCs. A post-mortem was carried out on the pregnant female killer whale, which was not in an advanced state of decay. It was discovered Analyses of PCBs and PBDEs for both adult female killer whales as that the foetus was female and in cranial presentation (Ryan and well as the foetus sample were carried out at the Marine Institute, ISO Pierini, 2013). No cause of death was established for any of the samples. 17025 accredited for the analysis of PCBs. NIST 1947 Lake Michigan The adult female from Tramore was in excellent condition, however the tissue was used as a certified reference material (CRM) and was ana- male from Roundstone was in poor condition with its skin lost to lysed alongside samples. LOQs across all analytes ranged from 0.05 to weathering and scavenging. No length measurement was taken of the 0.2 ng/g, a full list of LOQs can be found in the Supplementary male but it was estimated at around 7 m. Information. Procedural blanks were also run, and samples were ana- The Smedes method of extraction was used for the extraction of the lysed in triplicate. NIST 1947 Lake Michigan tissue was used as a CRM lipid component of the blubber samples (Smedes, 1999). This involved for this analysis. The adult male killer whale was analysed for PCBs, homogenization using an Ultra Turrax (IKA T25) and a solvent mix of PBDEs and OCs in the Galway-Mayo Institute of Technology.