Contamination by Persistent Organohalogen Compounds in Deep-Sea Fishes from Off the Pacifi C Coast of Northern Japan
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Deep-sea Fauna and Pollutants off Pacifi c Coast of Northern Japan, edited by T. Fujita, National Museum of Nature and Science Monographs, No. 39, pp. 737-755, 2009 Contamination by Persistent Organohalogen Compounds in Deep-sea Fishes from off the Pacifi c Coast of Northern Japan Shin Takahashi1*, Tomoko Oshihoi1, Tomohiko Isobe1, Karri Ramu1, Koji Ohmori1, Tsunemi Kubodera2 and Shinsuke Tanabe1 1 Center for Marine Environmental Studies, Ehime University, Bunkyo-cho 2̶5, Matsuyama, Ehime, 790̶8577 Japan E-mail: [email protected] 2 Department of Zoology, National Museum of Nature and Science, 3̶23̶1 Hyakunin-cho, Shinjuku-ku, Tokyo, 169̶0073 Japan Abstract: Twelve species of deep-sea fi shes collected in 2005 from off the Pacifi c coast of northern Japan from depths ranging from 400̶1000 m were analyzed for persistent organochlorine compounds (OCs), includ- ing PCBs and organochlorine pesticides and brominated fl ame retardants (BFRs) such as polybrominated di- phenyl ethers (PBDEs) and hexabromocyclododecane isomers (HBCDs). Among OCs, concentrations of DDTs and PCBs (up to 23000 and 12400 ng/g lipid wt, respectively) were the highest and other OCs were approximately in the order of CHLs > HCHs ≥ HCB. PBDEs and HBCDs were also detected in almost all the deep-sea fi shes. The present study is the foremost to report the occurrence of BFRs in deep-sea fi shes from the North Pacifi c region. Although magnitude of contamination by these organohalogen compounds in most of the fi sh species analyzed was comparable or lower than that reported in shallow-water and deep-sea fi shes from Japanese coastal waters, snubnosed eels accumulated some hydrophobic compounds like PCBs, DDTs and PBDEs at extremely high concentrations. Signifi cant positive correlations found between δ15N (‰) and PCBs, DDTs and PBDEs suggest the high biomagnifi cation potential of these contaminants in food web. Neverthe- less, large variation in δ13C (‰) values observed between the species indicate multiple sources of carbon in the food web and specifi c accumulation of hydrophobic organohalogen compounds in benthic dwelling species like snubnosed eel. It is noteworthy that no signifi cant declining trends of PCBs, HCB and HCHs levels were observed in fi shes collected in 1995 and 2005, suggesting continuous input of the contaminants into the envi- ronment. The results obtained in this study highlight the usefulness of deep-sea fi shes as sentinel species to monitor the deep-sea environment. Key words: organochlorines, brominated fl ame retardants, stable isotopes, deep-sea fi shes, Tohoku region Introduction The long-range transport, persistence, and global dynamics of persistent organic pollutants (POPs) are issues of increasing concern in recent years. Organochlorine compounds (OCs), a rep- resentative group of classical POPs, are ubiquitous contaminants entering the marine environment in coastal areas, mainly by river infl ow and continental runoff and in the open sea by atmospheric deposition. In the global marine environment, the apparent fate of these compounds is to adsorb to the detritus and marine snow and eventually carried to the deep-sea where they biomagnify in the food web (Froescheis et al., 2000). Several models suggested that deep-sea sediments are the fi nal accumulation site for OCs (Woodwell et al., 1971; Tatsukawa and Tanabe, 1984), and fi sh living in association with sediments are exposed to and accumulate these compounds (Berg et al., 1997). Increasing concern that the deep-sea might act as an ultimate sink for such contaminants and the growing importance of deep-sea commercial fi sheries around the world have resulted in numerous * To whom correspondence should be addressed. 738 Shin Takahashi et al. monitoring studies on the accumulation of OCs in deep-sea organisms (Berg et al., 1997, 1998; Lee et al., 1997; Takahashi et al., 1998, 2000, 2001; Looser et al., 2000; Froescheis et al., 2000; Sole et al., 2001; de Brito et al., 2002a; Mormede and Davies, 2003; Storelli et al., 2004). Al- though our previous study also found signifi cant levels of OC contaminants in some deep-sea or- ganisms collected from off the Pacifi c coast of northern Japan, during 1994-1995 (de Brito et al., 2002a), no recent information is available on the contamination status of OCs in the ecosystem of this region. In addition to OC contamination, aquatic pollution resulting from widespread usage of bro- minated fl ame retardants (BFRs) such as polybrominated diphenyl ethers (PBDEs) and hexabro- mocyclododecanes (HBCDs) deserves concern because of the bioaccumulation potential, persis- tence and endocrine disrupting effects of the contaminants (Watanabe and Sakai, 2003, Tanabe et al., 2008). Therefore, these compounds have been recently reported as emerging global environ- mental contaminants. Nevertheless, compared to OCs, there is still little information on contami- nation by BFRs in the Asia-Pacifi c region, and studies addressing the contamination of deep-sea areas by BFRs are scarce (Ramu et al., 2006). Concerned over the possible fl ux of such persistent organohalogen contaminants to the bot- tom of the oceans, the present study attempted to investigate the contamination and accumulation of OCs, such as polychlorinated biphenyls (PCBs), DDT and its metabolites (DDTs), chlordane- related compounds (CHLs), hexachlorocyclohexane isomers (HCHs) and hexachlorobenzene (HCB), and BFRs such as PBDEs and HBCDs, in deep-sea fi shes from off the Pacifi c coast of northern Japan (Tohoku region). Additionally, the data on OCs in deep-sea fi shes reported in our earlier study (de Brito et al., 2002a) were compared with that observed in this study to delineate the temporal trend of OCs contamination during the last decade from 1994/95 to 2005. Stable isotope analysis is generally used to investigate energy fl ow through an ecosystem. The δ15N and δ13C values in animals refl ect their diets. Thus, trophic relationships can successfully be derived using relative abundances of naturally occurring stable isotopes of nitrogen (15N/14N, expressed as δ15N values) (Hobson and Welch, 1992). Furthermore, measurements of δ15N as a continuous trophic-level variable enable to quantitatively estimate the magnitude of contaminant biomagnifi cation within food webs (Ruus et al., 2002). Hence, to examine the biomagnifi cation of OCs and BFRs through the deep-sea food web, δ15N and δ13C analyses were performed on deep- sea fi shes from off the Pacifi c coast of northern Japan. The present study was conducted as part of a joint research project entitled “Study on Deep- Sea Fauna and Conservation of Deep-Sea Ecosystem” between the Department of Zoology, Na- tional Museum of Nature and Science and Center for Marine Environmental Studies, Ehime Uni- versity. Materials and Methods Samples Twelve species of deep-sea fi shes collected from off the Pacifi c coast of northern Japan (36̶38˚N, 141̶142˚E) from depths ranging from 400 to 1000 m during October to November 2005 were analyzed in this study. The fi sh samples were collected by the R/V Wakataka-maru of the Fisheries Research Agency (FRA) using a research bottom trawl. Sampling location and biological information of the samples are shown in Fig. 1 and Table 1, respectively. The collected samples were placed in polyethylene bags and frozen in a deep-freezer at ‒25˚C until chemical analysis. The whole body of individual specimens belonging to the same species collected from the same sampling location were pooled and homogenized to prepare a composite sample for chemical analysis. Contaminants in Deep-sea Fishes from off Tohoku 739 Table 1. Sample details of deep-sea fi shes from off the Pacifi c coast of northern Japan. n.m: not measured. Sampling Depth Mean Mean Sample No. Common name Scientifi c name n Habitat year (m) length (cm) weight (g) Fish-1 Flathead fl ounder Hippoglossoides dubius 1 2005 650 37 610 Demersal Fish-2 Flathead fl ounder Hippoglossoides dubius 1 2005 650 36 500 Demersal Fish-3 Longfi n codling Laemonema longipes 1 2005 650 47 500 Bathydemersal Fish-4 Kaup’s arrowtooth eel Synaphobranchus kaupii 1 2005 550 67 450 Bathydemersal Fish-5 Kaup’s arrowtooth eel Synaphobranchus kaupii 1 2005 550 61 290 Bathydemersal Fish-6 Kaup’s arrowtooth eel Synaphobranchus kaupii 1 2005 550 69 610 Bathydemersal Fish-7 Spinyhead sculpin Dasycottus setiger 1 2005 450 26 290 Demersal Fish-8 Snubnosed eel Simenchelys parasitica 1 2005 900 44 140 Bathydemersal Fish-9 Snubnosed eel Simenchelys parasitica 1 2005 900 41 100 Bathydemersal Fish-10 Snubnosed eel Simenchelys parasitica 1 2005 900 36 65 Bathydemersal Fish-11 Snubnosed eel Simenchelys parasitica 1 2005 900 38 100 Bathydemersal Fish-12 Sake-bikunin Careproctus rastrinus 2 2005 425 n.m 160 Bathydemersal Fish-13 Longarm grenadier Coelorinchus macrochir 1 2005 410 59 620 Bathydemersal Fish-14 Longarm grenadier Coelorinchus macrochir 1 2005 410 59 720 Bathydemersal Fish-15 Largenose grenadier Coryphaenoides nasutus 5 2005 900 31 71 Bathydemersal Fish-16 Blackbelly lanternshark Etmopterus lucifer 3 2005 480 50 230 Benthopelagic Fish-17 Pacifi c cod Gadus macrocephalus 1 2005 450 39 610 Demersal Fish-18 Pacifi c cod Gadus macrocephalus 1 2005 450 38 760 Demersal Fish-19 Eelpout Lycodes hubbsi 2 2005 750 38 130 Bathydemersal Fish-20 Brokenline laternfi sh Lampanyctus jordani 14 2005 480 13 17 Bathypelagic Fig. 1. Map showing the sampling area (shaded portion) off the Pacifi c coast of northern Japan (Tohoku region). 740 Shin Takahashi et al. Chemical analysis Analysis of PBDEs and HBCDs was performed following the procedures described by Ueno et al. (2004, 2006) with slight modifi cations, while OCs such as DDTs, CHLs, HCHs, HCB, and PCBs were analyzed following the method described by Kajiwara et al. (2003). Briefl y, 15̶30 g of the homogenized tissue sample was ground with anhydrous sodium sulfate and extracted in a Soxhlet apparatus with a mixture of diethyl ether and hexane for 7̶8 h.