BRIEF COMMUNICATION PUBLISHED: 13 FEBRUARY 2017 | VOLUME: 1 | ARTICLE NUMBER: 0051 Bioaccumulation of persistent organic pollutants in the deepest ocean fauna Alan J. Jamieson1 *†, Tamas Malkocs2, Stuart B. Piertney2, Toyonobu Fujii1 and Zulin Zhang3 The legacy and reach of anthropogenic influence is most organisms have reported higher concentrations than in nearby clearly evidenced by its impact on the most remote and surface-water species11,12. However, although these studies are inaccessible habitats on Earth. Here we identify extraordi- described as ‘deep sea’, they rarely extend beyond the continental nary levels of persistent organic pollutants in the endemic shelf (< 2,000 m), so contamination at greater distances from shore amphipod fauna from two of the deepest ocean trenches and at extreme depths is hitherto unknown. (>10,000 metres). Contaminant levels were considerably We measured the concentrations of key PCBs and PBDEs in higher than documented for nearby regions of heavy indus- multiple endemic and ecologically equivalent Lysianassoid amphi- trialization, indicating bioaccumulation of anthropogenic con- pod Crustacea from across two of the deepest hadal trenches — the tamination and inferring that these pollutants are pervasive oligotrophic Mariana Trench in the North Pacific, and the more across the world’s oceans and to full ocean depth. eutrophic Kermadec in the South Pacific. Two endemic amphi- The oceans comprise the largest biome on the planet, with the pods (Hirondellea dubia and Bathycallisoma schellenbergi) were deep ocean operating as a potential sink for the pollutants and sampled from the Kermadec between 7,227 and 10,000 m, and one litter that are discarded into the seas1. The spatial and bathymetric (Hirondellea gigas) from the Mariana between 7,841 and 10,250 m. expanse of the deep sea infers that there are still large areas Samples were obtained using traps deployed on deep-sea landers13. untouched by anthropogenic activity, although the intrinsic link- The concentrations of seven PCB congeners identified by ICES14 for ages between the deep sea and surface waters2 would suggest this marine pollution assessment and seven PBDE congeners were mea- inference is ill-conceived3. The hadal zone (6,000 to 11,000 m deep) sured both in sample dry weight (dw) and lipid weight (lw). is comprised of trenches formed at tectonic subduction zones, and The salient finding was that PCBs and PBDEs were present in represents the least explored ecosystem on Earth and the last major all samples across all species at all depths in both trenches (Figs 1 marine ecological frontier4. Trenches have been considered as pris- and 2). The Σ PCB7 concentrations ranged from 147.3–905 ng g−1 dw tine environments, but also (given their locations and topography) in the Mariana and 18.03–42.85 ng g−1 dw in the Kermadec, as likely sinks for contaminants that enter the marine environment2. with mean values of 382.28 ng g−1 dw (±281.6 s.d.) and 25.24 ng g−1 dw Of particular concern are the persistent organic pollutants (POPs) (±9.1 s.d.), respectively. Across individual PCB congeners, that are highly detrimental to organismal health through their PCB 153 was detected in the highest concentration (mean 64.45, endocrine disrupting properties5. POPs possess an inherent hydro- range 5.03–373.63 ng g−1 dw). Congeners PCB 138 and 153 phobicity that confers a high binding affinity to organic or inor- alone accounted for 65% of the total PCB concentration, which ganic particles present in the water column that, through vertical suggested that the heavier congeners were more recalcitrant transport, will collect in the deep ocean. They also have inherent towards degradation. lipophilicity, meaning these compounds readily bioaccumulate in Σ PBDE7 concentrations ranged from 5.82–28.93 ng g−1 dw in organisms, with cumulative increases at each trophic level6. the Mariana Trench and 13.75–31.02 ng g−1 dw in the Kermadec. POPs were released into the environment through industrial Concentrations of congeners PBDE 153 and 154 were below the accidents and discharges, leakage from landfills, or incomplete limit of detection (LOD) in some samples, while PBDE 183 was not incineration7. Two key POPs are polychlorinated biphenyls (PCBs, detected at all. Congeners PBDE 47 and 99 were found the higher used as dielectric fluid) and polybrominated diphenyl ethers concentrations (mean: 8.81, range 2.55–21.36 ng g−1 dw; mean 3.31, (PBDEs, used as flame retardants). From the 1930s to when PCB range 0.78–8.38 ng g−1 dw, respectively) and accounted for 71% of production ceased in the 1970s, the total global production was the total PBDE concentration. ~1.3 million tonnes8. Approximately 65% is thought to be contained For both Σ PCB7 and Σ PBDE7 there were significant correla- in landfills or still within electrical equipment, with the other 35% tions between dry and lipid weights (Pearson’s r = 0.98, P = 8 × 10−9 residing in coastal sediments and open oceans9. These pollutants and r = 0.70, P = 0.012, respectively). There was no statistically are invulnerable to natural degradation10 and so persist in the envi- significant relationship between concentration and depth within ronment for decades. Moreover they can spread great distances, either trench (see Supplementary Information). In both trenches, including to seemingly isolated environments, such as polar regions the highest values were found in the upper trench; 7,841 m in the and the open ocean3. Mariana and 7,227 m in the Kermadec. Pollutants entering the deep sea are deposited in sediments and These data clearly indicate that potent anthropogenic con- can readily accumulate in the food chain11. Studies on deep-sea tamination and bioaccumulation has occurred in a dominant 1Oceanlab, Institute of Biological and Environmental Sciences, University of Aberdeen, Main Street, Newburgh, Aberdeenshire AB41 6AA, UK. 2Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK. 3The James Hutton Institute, Environmental and Biochemical Sciences, Craigiebuckler, Aberdeen AB15 8QH, UK. †Present address: School of Marine Science and Technology, Newcastle University, Ridley Building, Newcastle upon Tyne NE1 7RU, UK. *e-mail: [email protected] NATURE ECOLOGY & EVOLUTION 1, 0051 (2017) | DOI: 10.1038/s41559-016-0051 | www.nature.com/natecolevol 1 © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. BRIEF COMMUNICATION NATURE ECOLOGY & EVOLUTION ΣPCB7 (ng g–1) Kermadec Trench 0 250 500 750 1,000 1,250 1,500 1,750 2,000 H. dubia (7,227 m) B. schellenbergi (7,227 m) H. dubia (7,904 m) B. schellenbergi (7,904 m) H. dubia (9,005 m) Species and depth H. dubia (10,000 m) Dry weight Lipid weight Mariana Trench 0 250 500 750 1,000 1,250 1,500 1,750 2,000 H. gigas (7,841 m) H. gigas (7,912 m) H. gigas (8,028 m) H. gigas (8,847 m) H. gigas (8,942 m) Species and depth H. gigas (10,250 m) Dry weight Lipid weight Figure 1 | Polychlorinated biphenyl (PCB) concentration for both dry and lipid weight found in endemic hadal amphipods across the bathymetric ranges of the Kermadec and Mariana trenches. macrofaunal group inhabiting the complete depth range of two of the Trench are estuarine sediments from New Zealand’s North Island deepest marine trenches. Placing the levels of contamination into a (0.55 to 573 ng g−1 dw)21. These results are, however, highly vari- broader comparative context with values published from the western able with some locations — such as Puketutu Island, where levels Pacific is complicated by variations in POP congeners assayed across are exceptionally high (> 500 ng g−1 dw). However, the median different studies and level of replication. Notwithstanding, some value of 10.3 ng g−1 dw is considerably lower than the Kermadec insightful comparisons are possible. World baseline levels for Σ PCBs Trench (18.4 ng g−1 dw) and close to that in the Mariana Trench arising from atmospheric transport found in clean coastal sediments (10.44 ng g−1 dw). The levels of PBDEs from New Zealand estuar- are < 1 ng g−1 dw (ref. 15). In grossly polluted areas, levels can be far ies were not considered excessively high21. Nevertheless, the salient higher16, reaching up to 314 ng g−1 dw in Guam, 240 ng g−1 dw in Japan finding is that PBDEs are present in the hadal samples at compa- and 160 ng g−1 dw in Australia17. Indeed, in the Mariana, the highest rable or higher levels than in coastal waters. levels of PCBs were fifty times more contaminated than crabs from PCB concentrations were notably higher in the Mariana than in paddy fields fed by the Liaohe River, one of the most polluted rivers in the Kermadec Trench. There are several possible explanations that China18. The only Northwest Pacific location with values comparable are not mutually exclusive and, at this juncture, speculative. First, to the Mariana Trench is Suruga Bay (Japan), a highly industrialized the high levels of the Mariana PCBs may originate from proxim- area with historically heavy usage of organochlorine chemicals19. ity to the industrialized regions in the Northwest Pacific22 and the Contamination by PBDEs did not reach the magnitude of North Pacific Subtropical Gyre, famed for its reputation as the PCB levels20. The closest data for PBDE levels to the Kermadec ‘Great Pacific Garbage Patch’23. As such, it is located beneath a mass ΣPBDE7 (ng g–1) Kermadec Trench 050 100 150200 250300 350 H. dubia (7,227 m) h B. schellenbergi (7,227 m) H. dubia (7,904 m) B. schellenbergi (7,904 m) H. dubia (9,005 m) Species and dept Dry weight Lipid weight H.