Environ. Sci. Technol. 2010, 44, 5741–5747
Marine Natural Products, the Halogenated 1′-Methyl-1,2′bipyrroles, Biomagnify in a Northwestern Atlantic Food Web K R I S T I N C . P A N G A L L O * ,†,‡ A N D CHRISTOPHER M. REDDY‡ Department of Biochemistry and Microbiology, Rutgers, The State University of New Jersey, 76 Lipman Road, New Brunswick, New Jersey 08901, and Department of Marine Chemistry & Geochemistry, Woods Hole Oceanographic Institution, 360 Woods Hole Road, Woods Hole, Massachusetts 02543
Received April 1, 2010. Revised manuscript received May 14, 2010. Accepted June 3, 2010.
Halogenated 1′-methyl-1,2′-bipyrroles (MBPs) are putative marine natural products that accumulate in marine mammal blubber in similar concentrations and patterns to biomagnifying organic pollutants. Here we measure concentrations of MBPs and 2,2′,4,4′,5,5′-hexachlorobiphenyl (CB-153) in 40 samples composed of eight fish species, two squid species, and six species of marine mammals. To determine their trophic positions and to further investigate influence of prey preference, we also measured the stable carbon and nitrogen isotopic compositions of all samples. Our results show that lipid-normalized MBP concentrations increase with increasing trophic level; therefore, MBPs qualify as another class of biomagnifying marine natural products. The presence of MBPs in pinniped prey and absence in pinniped blubber suggests that these mammals share dietary exposure to MBPs with odontocetes but have an enhanced ability to metabolize these natural products.
1. Introduction Halogenated 1′-methyl-1,2′-bipyrroles (MBPs) are putative marine natural products present in the tissues of marine mammals and other species occupying the highest trophic levels of marine food webs (1–3). They are unusual among the halogenated natural products (HNPs) in their N,C1linkage, which is thus far undocumented in other naturally produced bipyrroles, and their degree of halogenation. The most abundant MBPs in environmental samples contain six or seven halogens (2, 3). Due to the number of halogens and their structure, MBPs have high estimated octanol-water partition coefficients (Kow ) 107.2-108.3) (4) and preferentially partition into lipid-rich reservoirs, such as blubber. These characteristics make them very similar to the persistent organic pollutants (POPs), and in this respect they are an untapped resource. By studying the pathways and fate of these HNPs, we can better understand the ultimate fate of POPs in the marine environment. The concern over POPs is due to their negative impacts on human and environmental health (5, 6) and also to their recalcitrance. The persistence of these compounds results * Corresponding author e-mail:
[email protected]. † The State University of New Jersey. ‡ Woods Hole Oceanographic Institution. 10.1021/es101039d
2010 American Chemical Society
Published on Web 06/28/2010
in elevated concentrations in some reservoirs, especially soil and sediment, despite strict environmental regulation in the past decades (7, 8). Thus, these compounds continue to circulate within food webs, and concentrations remain high in top predators (9). These high concentrations result from biomagnification, which is the increase in lipid-normalized contaminant concentrations with increasing trophic level resulting from trophic transfer (10). Thus, predators have contaminant concentrations that are higher than what would be expected based on equilibrium partitioning between the surrounding environment (i.e., water, sediment) and biotic tissues (10). The mechanisms and time-scales for removal of these contaminants from the biosphere are not yet clear (11). Due to their structural similarities to POPs, it was suspected that some HNPs biomagnify; this has been confirmed for halogenated 1,1′-dimethyl-2,2′-bipyrroles (DMBPs) (12) and methoxylated polybrominated diphenyl ethers (MeO-PBDEs) (13). Biomagnifying HNPs have evolved with their ecosystem and, presumably, have established routes of entry (biosynthesis) and exit (degradation and/or physical removal - e.g., burial). In fact, the enzymes responsible for POP degradation may have evolved to degrade HNPs (14). Previous work has suggested that MBPs may be another type of biomagnifying natural product (3). MBPs are present in marine mammal blubber in similar concentrations and in similar patterns to POPs known to biomagnify (3). Additionally, MBPs have been detected in marine mammal prey (squid) (15, 16), fish oil (17), and human breast milk (18), suggesting that these compounds are transferred through food. Here we demonstrate that the lipid-normalized concentration of MBPs increase with trophic level in the Northwestern Atlantic Ocean. In doing so, we have newly detected MBPs in eight species, many of which are commonly consumed by people.
2. Methods 2.1. Sampling. The 20 marine mammals analyzed in this study consist of both odontocete cetaceans (toothed whales) and pinnipeds (earless seals). The odontocete samples include seven common dolphins (Delphinus delphis), four Atlantic white-sided dolphins (Lagenorhynchus acutus), one harbor porpoise (Phocoena phocoena), and one long-finned pilot whale (Globicephala melas). The pinniped samples are two gray seals (Halichoerus grypus) and five harp seals (Phoca groenlandica). All the samples were acquired through the Cape Cod Stranding Network, 18 were fatally stranded on Cape Cod from 2004-2007, and 2 were caught in fishing gear (the harbor porpoise and one gray seal) just south of New England. Only those animals characterized as “fresh dead” were used for the study to minimize any effect of tissue decomposition. For additional details on the individual marine mammals, including weight, length, age, and nutritional status, see Table S1 and ref 3. The 20 fish and squid analyzed in this study were obtained from the 2007 Fall Bottom Trawl Survey conducted by the National Marine Fisheries Ecosystems Survey Branch (Woods Hole, MA). Species were selected based on their role as marine mammal prey: longfin inshore squid (Loligo pealeii), northern shortfin squid (Illex illecebrosus), Atlantic herring (Clupea harengus), Atlantic mackerel (Scomber scombrus), white hake (Urophycis tenuis), red hake (Urophycis chuss), silver hake (Merluccius bilineariz), Acadian redfish (Sebastes fasciatus), Atlantic cod (Gadus morhua), and haddock (Melanogrammus aeglefinus). The samples were collected opportunistically during the survey, and approximately 1 kg (wet weight) of VOL. 44, NO. 15, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Lipid-Normalized Whole Body Concentrations (ng g-1 lipid) of Quantifiable MBPs and CB-153 in Nonmammalian Samples sample IDa (analytical error) MDL (ng µL-1)
Br7-MBP-79 ((4%) 2.0
MBP-Br6Cl-b ((9%) 2.2
MBP-Br6-b ((5%) 0.87
MBP-Br5Cl-d ((6%) 1.1
MBP-Br5Cl-e ((24%) 0.6
MBP-Br5Cl-f ((6%) 0.2
CB-153 ((10%) 0.26
Loligo 121 Loligo 89 Illex 87 Illex 178 Herring 228 Herring 219 Mackerel 244 Mackerel 268 White Hake 275 White Hake 299 Red Hake 168 Red Hake 169 Silver Hake 176 Silver Hake 165 Acadian Redfish 258 Acadian Redfish 257 Cod 326 Cod 324 Haddock 214 Haddock 205
