Environ. Sci. Technol. 2008, 42, 1058–1065
Bioturbation-Driven Release of Organic Contaminants from Baltic Sea Sediments Mediated by the Invading Polychaete Marenzelleria neglecta M A R I A E . G R A N B E R G , * ,† JONAS S. GUNNARSSON,‡ JENNY E. HEDMAN,‡ RUTGER ROSENBERG,† AND PER JONSSON§ Göteborg University, Department of Marine Ecology, Kristineberg Marine Research Station, 450 34 Fiskebäckskil, Sweden, Stockholm University, Department of Systems Ecology, 106 91 Stockholm, Sweden, and Stockholm University, Department of Applied Environmental Sciences (ITM), 106 91 Stockholm, Sweden
Received June 30, 2007. Revised manuscript received October 21, 2007. Accepted October 31, 2007.
Baltic Sea sediments are among the world’s most polluted regarding eutrophication and contamination. Eutrophicationinduced hypoxia has caused depletion of bioturbating macrofauna in vast areas, producing laminated sediments. We investigated if reoxygenation and colonization by the invading deepburrowing polychaete Marenzelleria neglecta may cause an augmented contaminant release from Baltic Sea sediments. Intact laminated sediment cores were exposed either to in situ hypoxia, reoxygenation, or reoxygenation combined with bioturbating M. neglecta. The release fluxes of particleassociated (NPart) and dissolved (NDiss) PCBs and chlorinated pesticide residues (POPs) were quantified (GC-ECD) after 85 d along with contaminant concentrations in sediment and biota. Lavoisier-based mass transfer coefficients (Kf) were calculated from NDiss. Sediment contaminant concentrations were high (ΣPCB7: 42–52 ng gsediment-1 dw) due to emissions from Stockholm. NDiss always exceeded NPart by an order of magnitude. Bioturbation enhanced NDiss and Kf from hypoxic sediments 0.7 – 3 times while reoxygenation alone had no significant effect. M. neglecta accumulated low amounts of contaminants but significantly stimulated aquatic release of bioavailable sequestered contaminants. Bioturbation should be included in aquatic contaminant fate models. We advise to consider quiescent pollutant sources and possible ecological shiftswhenaimingtorestoreeutrophicatedaquaticenvironments.
Introduction During the 20th century, the semienclosed Baltic Sea has received increasing loads of nutrients and contaminants, turning it into one of the world’s most polluted seas (1). * Corresponding author phone: +45 46301267; fax: +45 46301114; e-mail:
[email protected]. † Göteborg University. ‡ Stockholm University, Department of Systems Ecology. § Stockholm University, Department of Applied Environmental Sciences. 1058
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Recently, bordering countries have taken joint measures to reduce the input of both contaminants and nutrients. The banning of DDT and PCBs in the 70s has, e.g. lead to the recovery of the Baltic Sea seal population (2), while eutrophication-related ecosystem disruptions, e.g. more frequently occurring toxic algal blooms, spreading of filamentous algae and oxygen deficiency in bottom waters, have proven more difficult to reverse. Extended periods of anoxic/hypoxic conditions in bottom waters have led to depletion of bioturbating macrofauna and subsequent spreading of laminated sediments in the Baltic Sea (3), and Jonsson et al. (4) estimate that up to 30 tons of PCBs may be stored in these sediments. Theoretical mass balance calculations performed on the current dynamics of persistent organic pollutants (POPs) in the Baltic Sea consider sediments as net sinks (e.g., refs 5, 6.). These studies, however, assume continuous equilibrium conditions between sediment and water phases, and the mass balance calculations do not close (7). In natural sediments biogeochemical equilibria are frequently disrupted by physical and biological disturbances. Physical disturbance is generally considered the dominant process causing release of sediment-associated contaminants. Recent studies do, however, suggest that bioturbation-driven release of dissolved (soluble) contaminants may be an equally, or even more important process (8, 9). Since POPs are particle reactive with a preference for sedimentary organic matter, macrofaunal feeding, particle-mixing and irrigation strongly affects the fate of sediment associated POPs (10). It is, however, in the dissolved (soluble) form that POPs are available for uptake in organisms (11). Desorption from particles occurs in deposit feeder guts and in the sediment. The mechanism behind a bioturbation-driven soluble release of contaminants from sediments, described by Thibodeaux and Bierman (12), involves initial bioturbation-aided transport of particleassociated contaminants to the sediment-water interface, followed by rapid desorbtion and subsequent diffusion through the benthic boundary layer into overlying waters. The fate of POPs is also determined by the composition of the sediment matrix, where contaminant affinity increases with the degree of organic matter refractority (13). The sedimentary oxygen regime affects organic contaminant degradation directly and indirectly by determining organic matter distribution and degradation rates (14–16). An important issue in the process of reversing eutrophication in the Baltic Sea is thus whether laminated sediments will start acting as contaminant sources when being aerated and recolonized by bioturbating organisms. A recently introduced invading polychaete genus Marenzelleria (spionidae), consisting of three currently identified species, i.e., M. viridis, M. neglecta, and M. arctia, is successfully colonizing and even dominating sediments of the North and Baltic Seas (17, 18). Due to its strong salinity gradient and comparably recent history, the Baltic Sea is species-poor with many unsaturated ecological niches. These conditions make the Baltic Sea particularly sensitive to exotic invasions (19). The dominating species M. neglecta and M. viridis are the first nonindigenous species with the ability to colonize sediments ranging from the shallow littoral to the deeper subhalocline soft bottoms of the Baltic Sea (20). Their successful establishment, with localized maxima of 30–40000 ind. m-2 (21), is mainly attributed to a physiological ability to cope with poor oxygen and high sulfide conditions in organically enriched environments (22, 23). Marenzelleria spp. reside in unbranched burrows reaching sediment depths of 40 cm (24), which is 10–35 cm deeper than the bioturbation depths of indigenous Baltic Sea infauna (25, 26). The feeding 10.1021/es071607j CCC: $40.75
2008 American Chemical Society
Published on Web 01/15/2008
behavior of M. neglecta is poorly documented, yet it appears to both subsurface and surface deposit feed ((27), Granberg unpublished data). M. neglecta exclusively defecates on the sediment surface, leaving string-like faecal casts. When feeding and burrowing, M. neglecta thus transfers contaminated particles from various depths to the sediment surface, while its irrigation creates well oxygenated burrow linings. Upward conveying, intermittent shallow biodiffusing, and bioirrigating behaviors (28) may summarize the observed bioturbation patterns by M. neglecta. The establishment of Marenzelleria spp. in areas with contaminated laminated sediments may consequently stimulate mobilization of sediment-associated contaminants, which until now have been safely sequestered and kept out of circulation. We present results from an experimental study investigating the effects of reoxygenation and bioturbation caused by Marenzelleria neglecta on the release of POPs from naturally contaminated laminated hypoxic Baltic Sea sediments. The main research objectives were to investigate if contaminant release (i) was affected by reoxygenation, (ii) was affected by combined reoxygenation and bioturbation by M. neglecta, and (iii) mainly would be in a particleassociated or dissolved form.
Materials and Methods Collection of Sediment and Organisms. Laminated sediments were collected from R/V Sunbeam, in the inner Stockholm archipelago (59°21′100, 18°15′450) from 30 m depth using a Gemini twin gravity corer with two Perspex tubes (inner diameter: 8 cm, length: 89 cm). Only sediment cores with undisturbed surfaces and clear water columns were retained. On the ship, the sediment cores were topped with bottom water collected at the same site (Ruttner sampler) and sealed, then transported to Kristineberg Marine Research Station (KMRS), Göteborg University, Sweden, where they were stored dark and cold (in situ temperature +8 °C) until experimental start. Additional Baltic Sea water (7 PSU) for the experimental systems was collected from 37 m depth at Studsvik field station, Stockholm University, Sweden. Marenzelleria neglecta were collected in the outer Darss-Zingst estuary, southern Baltic Sea, Germany, using an EkmannBirge grab. The polychaetes were hand-picked by gentle wetsieving (0.5 mm mesh size) and transported to KMRS in aerated insulated tanks containing a thin sediment layer (2 cm) and seawater (5 PSU), collected at the sampling site. At KMRS the polychaetes were kept in aquaria with sediment and aerated seawater (5 PSU, 8 °C) in darkness for one week, until experiment start. Experimental Design and Setup. Sediment cores were exposed to either of three treatments (n ) 4): continued exposure to hypoxic (
