Download      Fate of contaminants in Baltic Sea sediment ecosystems:   the role of bioturbation

 Fate of contaminants in Baltic Sea sediment ecosystems: the role of bioturbation Jenny E Hedman Doctoral Thesis in Marine Ecotoxicology ©Jenny Hedman, Stockholm 2008
Department of Systems Ecology, Stockholm University, SWEDEN
ISBN 978-91-7155-775-9
Printed in Sweden by US-AB, Stockholm 2008
Cover illustration by Frøydis Hellem and Jenny Hedman
-2-
-3-
Till mamma och pappa -4-
ABSTRACT Aquatic sediments are of major importance for the cycling of environmental
pollutants, acting as both sinks and secondary sources of contaminants to the
ecosystem. Sediment-living organisms can affect the fate and transport of
contaminants through activities like feeding and burrowing, collectively called
bioturbation. Apart from high contaminant levels, the Baltic benthic ecosystem is
affected by stressors such as eutrophication-induced anoxic conditions and invading
alien species. The main objectives of this thesis were to determine the effects of
bioturbation on contaminant fluxes in Baltic Sea sediments and to increase the
understanding of how these other stressors act together upon contaminant fate in the
benthic ecosystem.
Bioturbation affected contaminants in a species-specific way. The native species
Monoporeia affinis and Macoma balthica increased the incorporation of BDE-99
and Cd deposited on the sediment surface, enhancing their retention in the sediment.
The invasive polychaete Marenzelleria sp. did not contribute to the incorporation of
surface-deposited contaminants, however, significantly increased the release of
contaminants back to the water column. Reoxygenation of anoxic laminated
sediments and bioturbation by Marenzelleria increased the sediment-to-water flux
of dissolved organic contaminants. When the bioturbation-driven release of PCB
was compared to the release caused by physical sediment resuspension, results
indicated that the continuous activities of benthic infauna can be just as, or even
more, important than physical disturbance for the remobilization of sediment-bound
contaminants. Bioaccumulation was significantly higher when contaminants were
deposited associated to phytoplankton compared to lignin or sediment, suggesting
that there are likely seasonal differences in the mobilization of contaminants in the
benthic ecosystem.
In summary, bioturbation is an important process influencing contaminant fate in
Baltic Sea sediments, and the risk of remobilization of historically buried
contaminants may increase with improved benthic redox conditions and the
invasion of new deeper-digging species, such as Marenzelleria.
-5-
LIST OF PAPERS This thesis is based on the following five papers, referred to in the text by their
roman numerals.
I
Hedman JE, Bradshaw C, Thorsson MH, Gilek M, Gunnarsson JS (2008).
Fate of contaminants in Baltic Sea sediments: role of bioturbation and settling
organic matter. Marine Ecology Progress Series 356: 25-38.
II
Thorsson MH, Hedman JE, Bradshaw C, Gunnarsson JS, Gilek M (2008).
Effects of settling organic matter on the bioaccumulation of cadmium and
BDE-99 by Baltic Sea benthic invertebrates. Marine Environmental Research
65: 264-281.
III
Hedman JE, Stempa Tocca J, Gunnarsson JS (Manuscript). Remobilization of
PCB from Baltic Sea sediment: comparing the roles of bioturbation and
physical resuspension. Submitted to Environmental Toxicology & Chemistry.
IV
Granberg ME, Gunnarsson JS, Hedman JE, Rosenberg R, Jonsson P (2008).
Bioturbation-driven release of organic contaminants from Baltic Sea
sediments mediated by the invading polychaete Marenzelleria neglecta.
Environmental Science & Technology 42: 1058-1065.
V
Hedman JE, Gunnarsson JS, Samuelsson G, Gilbert F. Sediment particle
reworking and solute transport by two common polychaetes in the Baltic Sea,
Nereis diversicolor and Marenzelleria sp. (Manuscript)
My contribution to the papers: (I) – experimental design and execution, major part of the chemical
analyses, data analysis, most of the writing. (II) – experimental design and execution, participated in the
chemical analyses and writing. (III) – experimental design, major part of the experimental execution,
chemical analyses and data analysis, all writing. (IV) – contaminant analysis (GC-ECD) of extracts,
participated in data analysis and writing. (V) – participated in the experimental execution, bromide
analysis, most of the writing.
Published papers are reprinted with the kind permission of the publishers.
-6-
TABLE OF CONTENTS ABSTRACT ……………………………………………………………………..…… 5 LIST OF PAPERS ……………………….…….…………………………….………… 6 INTRODUCTION ……………………….…….…………………………….………… 8 Scope and aims of the thesis FATE OF CONTAMINANTS IN SEDIMENT ECOSYSTEMS ………………………….……….. 10 Contaminant properties and partitioning between media Transport processes at the sediment‐water interface Chemical and physical processes Macrofauna activities Uptake in organisms WHAT’S SO SPECIAL ABOUT THE BALTIC SEA? ….…………………………….………… 16 METHODS AND STUDY ORGANISMS …….…….…………………………….………… 18 PAPERS IN BRIEF ‐ RESULTS …………….…….…………………………….………… 22 Fate of surface deposited contaminants Paper I and II: Interactive effects between bioturbation and settling organic matter Remobilization of sediment‐associated contaminants Paper III: Comparing bioturbation and physical resuspension Paper IV: The effect of oxygenation and recolonisation of laminated sediments Bioturbation mechanisms Paper V: Particle and solute transport by two polychaetes DISCUSSION ………….…………….…….……………………………...………… 26 Bioturbation and the fate of contaminants in the Baltic Sea The multiple roles of organic matter for contaminant fate Potential effects of the invasion of Marenzelleria CONCLUSIONS ………….…………….…….……………………………...……… 30 ACKNOWLEDGEMENTS ….…………….…….…………………….………...….…… 31 REFERENCES ………….…………….…….……………..………….……....……… 33 -7-
INTRODUCTION An extensive amount of organic and metal contaminants has been released into the
environment as a consequence of the worldwide industrialization and urban
development. To determine and predict the risk of adverse effects of these
contaminants in the ecosystem, including human health, it is important to have a
good understanding of the processes that affect their environmental fate, i.e. their
distribution between media (e.g. air, water, soil/sediment) and ultimate removal
from the ecosystem. Generally, the fate of a contaminant in the environment can be
assessed by its physicochemical properties. However, the environment is inherently
dynamic, both in space and time, with complex interactions between abiotic and
biotic processes that make the fate of a contaminant increasingly difficult to predict
(and a lot more interesting!) when including ecological factors.
Aquatic sediments are of major importance for the global cycling of environmental
contaminants. Many persistent organic pollutants (POPs) and metals have a strong
affinity for particles and tend to accumulate in the seabed. Their burial deeper into
the sediment matrix is an important process in removing them from the ecosystem,
and sediments are thus often their final deposit. Nevertheless, the large amount of
contaminants stored in these sediments clearly also makes them potential secondary
sources to the ecosystem. Sediment-living organisms have a profound influence on
the biogeochemical properties of their habitat through activities such as feeding and
burrowing, collectively called bioturbation (Aller 1982). This also significantly
affects the bioavailability, degradation and transport of sediment-associated
contaminants (Forbes & Forbes 1994).
Scope and aims of the thesis This thesis focuses on the role of benthic macrofauna for the fate1 of contaminants
in Baltic Sea sediment ecosystems. The Baltic Sea suffers from several
anthropogenic stressors, including contamination by hazardous substances and
eutrophication, as well as the invasion of non-indigenous species. Separately, each
of these stressors has caused adverse effects in the Baltic ecosystem but there are
also interactive effects that influence the fate of contaminants in the benthic system.
The main aims of the thesis were to determine the effects of bioturbation on
-8-
contaminant fluxes in Baltic Sea sediments and to increase the understanding of the
complex interactions between ecological (e.g. bioturbation, organic matter cycling)
and physicochemical processes (e.g. contaminant partitioning) when assessing
contaminant fate in aquatic ecosystems.
The thesis is based on 5 experimental studies, paper I-V. In the first two papers (I,
II) the interactive effects of macrofauna activity (bioturbation and feeding) and
settling organic matter for the fate of newly deposited contaminants were examined.
The aim was to investigate how organic matter of different nutritional qualities
would stimulate infaunal feeding and bioturbation and thereby affect the overall fate
of the associated contaminants. Contaminants used in paper I and II were the metal
cadmium and the brominated flame retardant BDE-99. The following two papers
(III, IV) investigated the role of sediment as a source of historically buried
contaminants. In paper III the effect of bioturbation by common Baltic infauna was
compared to simulated physical resuspension for the sediment-to-water release of a
polychlorinated biphenyl (PCB). In paper IV the aim was to study the effects of
reoxygenation and recolonisation on the release of POPs from naturally
contaminated sediments, imitating the recovery from eutrophication induced anoxic
bottom water conditions. In paper I-IV, three common Baltic species with different
functional traits were used: the amphipod Monoporeia affinis, the clam Macoma
balthica, and the polychaete Marenzelleria sp. The polychaete genus Marenzelleria
is invasive in the Baltic Sea and has changed the benthic community structure in
many areas. In order to gain more knowledge about the mode and rate of
bioturbation by this worm, the mechanistic transport of particles and solutes by
Marenzelleria sp. and another polychaete, Nereis (Hediste) diversicolor, was
investigated and compared in paper V.
______________________
1
In this thesis, fate refers to the distribution of contaminants between compartments making up the
sediment ecosystem, simplified as sediment, overlying water and organisms. Since all work has been
done with POPs or a trace metal (cadmium), a discussion of contaminant degradation or metabolism is
not included here, although for many pollutants (even for POPs on longer time scales) it may be the most
important process for detoxification and removal from the ecosystem.
-9-
FATE OF CONTAMINANTS IN SEDIMENT ECOSYSTEMS Contaminants enter the aquatic environment through atmospheric deposition or via
rivers, land run-off and direct discharges. Air-water exchange is the dominating
process in the open ocean, and the association to sinking particulate organic matter
is a driving mechanism of contaminant removal from the water column (Wania &
Daly 2002). Contaminants entering with land discharges are often already sorbed to
suspended particles and their immediate fate in coastal waters is thus affected by the
hydrological transport and deposition of particles. The natural process of
sedimentation and the high particle affinity of contaminants result in the
accumulation of contaminants in aquatic sediments, often to concentrations several
orders of magnitude higher than in water, which makes sediments important sinks.
Contaminant properties and partitioning between media The behavior of a given contaminant in the environment is largely controlled by its
physicochemical properties (Schwarzenbach et al. 2003). Based on these properties
it will interact/react with various environmental constituents and partition between
compartments (e.g. air, water, sediment). This is important for environmental
transport processes and resistance to degradation, as well as for the bioavailability
and potential toxicity to living organisms.
Many different compound classes belong to the group of POPs. Some of the most
well-known members are chlorinated hydrocarbons, including polychlorinated
biphenyls (PCBs), dioxins, and organochlorine pesticides like DDT. Recently a
range of brominated organic compounds has been added to the list, e.g. the
polybrominated diphenyl ethers (PBDEs) commonly used as flame retardants (de
Wit 2002). POPs have a high resistance to chemical and biological degradation and
consequently a long environmental half-life. They are often nonpolar compounds
with a low solubility in water but with a high affinity for solid phases
(Schwarzenbach et al. 2003). In the aquatic environment, therefore, they rapidly
escape the water phase by adsorbing to (adsorption) or diffusing into particles
(absorption), both processes are jointly called sorption (Pignatello & Xing 1996).
Organic matter (OM) is generally the most important sorbent for hydrophobic
organic contaminants (HOCs) in the environment (Karickhoff et al. 1979). There is
- 10 -
a large variety in the sorption properties of OM for HOCs and much work has been
done to examine how the OM structure affects sorption/desorption processes
(Grathwohl 1990, Pignatello & Xing 1996, Cornelissen et al. 2005). Generally, it is
suggested that contaminants are more strongly associated with aged and/or
condensed OM than with fresh amorphous OM (Allen-King et al. 2002, Huang et
al. 2003). In addition, the sorption strength of HOCs generally increases with
increasing Kow - a measure of compound hydrophobicity (Karickhoff et al. 1979,
Chou & Griffin 1986), which has important implications for the environmental
transport and bioavailability of individual HOCs.
Partitioning of metal contaminants (such as Cd, Zn, Hg, Pb) in the aquatic
environment is a more complex process than for HOCs because metals can
associate with both organic and inorganic elements in several different ways, e.g. by
adsorption and complexation, as well as co-precipitate to form discrete particulates
(Santschi et al. 1997). All of these processes are highly sensitive to changes in the
abiotic environment, such as redox state, pH and salinity (Chapman et al. 1998). In
aerobic
environments,
adsorption
to
OM
and
iron
and
manganese
oxides/hydroxides is the predominant process, while under anoxic conditions the
formation of insoluble metal sulfides controls the dissolved fraction (Di Toro et al.
1990).
Transport processes at the sediment‐water interface Chemical and physical processes Sedimentation and resuspension of particles are important processes affecting the
fate of contaminants in benthic environments. In the absence of mixing (physical or
biological), continuous deposition of new sediment layers will eventually isolate
contaminants in deeper layers and reduce the risk of remobilization and exposure to
organisms. If the newly deposited material is clean or holds significantly lower
contaminant concentrations, the sediment quality will gradually improve (Wang et
al. 2004). However, before reaching an area where the hydrographical conditions
are stable enough to promote long-term accumulation, particles usually go through
a series of resuspension and relocation events (Jonsson 2000). Physical
resuspension and advective transport of contaminated sediment particles are key
- 11 -
processes in the large-scale fate of contaminants, and numerous field studies have
provided evidence for the importance of sediment resuspension for the transport and
internal recycling of HOCs and trace metals in aquatic ecosystems (Baker et al.
1985, Ko et al. 2003). Apart from the mass transport of particles and associated
contaminants, resuspension also increases the risk of contaminant exposure to
pelagic organisms (Eggleton & Thomas 2004). Resuspended sediment particles are
exposed to a new chemical environment which may promote desorption and release
of associated contaminants into the aquatic phase as truly dissolved chemicals
(Gong et al. 1998).
The release of dissolved contaminants from sediment to water involves three steps;
1) desorption from particle to pore water, 2) transport to the sediment-water
interface, and 3) diffusive transport over the boundary layer (Fig 1). The slowest
step in this sequential process determines the rate of release (Ortiz et al. 2004). For
POPs, slow desorption is often the limiting factor in the release, particularly for
very hydrophobic compounds, while for metals, partitioning is largely a function of
the sediment redox condition. Undisturbed sediments usually consist of a thin (mm)
oxidized surface layer over anoxic bulk sediment, which is due to the rapid
consumption of oxygen penetrating from the overlying water by chemical and
microbial processes in the sediment. The pore water concentration of metal
contaminants in those sediments is thus largely controlled by the presence of
sulfides and OM (Morse & Luther 1999). Advective pore water transport of solutes
within the sediment and to the sediment-water interface can be of great importance
in permeable sediments, however, in fine-grained cohesive sediments, which is
where contaminants often accumulate, advective pore water transport is negligible
and is instead dominated by molecular diffusion (Huettel & Gust 1992). Before
reaching the overlying water, contaminants have to pass through the diffusive
benthic boundary layer (DBL), a sub-layer close to the sediment surface where
turbulent mixing of the overlying water is approaching zero and compounds can
only pass this thin boundary layer by molecular diffusion (Boudreau 2001).
Diffusion over the benthic boundary layer is driven by the concentration difference
between the sediment pore water (Cpw [ng L-1]) and the overlying water (Cw). The
flux (N [ng m-2 d-1]) of a dissolved contaminant from sediment to water can
therefore be expressed by:
- 12 -
N = Kf · (Cpw – Cw)
Where Kf is the mass transfer coefficient (MTC [cm d-1]) describing the rate of
diffusion over the boundary layer, which is inversely proportional to the length of
the diffusive path, i.e. here the thickness of DBL (usually < 1 mm). The boundary
layer thickness is affected by several physical factors, such as current velocity and
sediment surface roughness, thus also altering the rate of transfer. MTCs are
determined empirically in laboratory experiments or field studies, and are often
used in chemical-fate models to predict the flux of dissolved contaminants from
sediment to water (Erickson et al. 2005).
Turbulent flow
Cw
Overlying water
Boundary layer
Sediment
Cpw
Pore
Fig 1. Schematic representation of soluble release of PCB from sediment to water.
Macrofauna activities There is a tight coupling between the organisms making up the benthic community
and the biogeochemical properties of the sediment, also affecting the fate of
deposited contaminants (Forbes & Forbes 1994). Sediment-living organisms have
developed a wide variety of different behavioral and feeding strategies in order to
adapt to and interact with their living environment. Bioturbation is the reworking of
the upper sediment layer (typically top 10 cm) by infauna from activities like
feeding, burrowing and the creation and ventilation of biogenic structures (e.g.
tubes, burrows). This biological mixing and transport of particles and solutes
profoundly affects various chemical and microbial processes within the sediment,
such as organic matter decomposition and inorganic nutrient regeneration, as well
as physical characteristics like porosity and sediment surface topography
(Kristensen et al. 1992, Aller & Aller 1998, Reise 2002). Benthic organisms can be
- 13 -
divided into functional groups based on how they mix particles and on whether and
how they irrigate the sediment (Francois et al. 2002, Gerino et al. 2003). Some
species randomly mix the sediment as they freely move around searching for food
(i.e. biodiffusors), whereas others are stationary and transport particles
unidirectional from one place to another (‘non-local transport’), e.g. by feeding at
depth and defecating digested material on the sediment surface (i.e. conveyors).
This mixing and transport of particles generally increase the rate of burial of surface
deposited contaminants and thus potentially enhance their retention in the sediment
(Petersen et al. 1998, Sandnes et al. 2000). On the contrary, they may also bring
back old pollutants to the top sediment layer, which slows down the burial and
increases the risk of remobilization to the water (Ciarelli et al. 1999). Particlebiodiffusion can also significantly increase the erodability of the sediment and
contribute to a higher release of contaminants even at low shear stress (Ciutat et al.
2006). Many species create permanent or semi-permanent tubes and burrows that
extend well into the anoxic bulk sediment. To meet respiratory needs and to avoid
toxic effects from exposure to sulfides in the anoxic pore water, these organisms
must ventilate their burrows (i.e. bio-irrigators) with oxic water from above the
sediment surface (Riisgård & Larsen 2005). This creates oxic micro-environments
within the sediment matrix that can oxidize metal sulfides and trigger microbial
mineralization of OM in the sediment (Heilskov & Holmer 2003), both of these
processes can increase the release of sorbed contaminants. The creation of burrow
structures extends the sediment-water surface area considerably and exposes
previously buried particle-associated contaminants at depth, increasing the area
available for diffusional processes (Aller & Aller 1998). Active burrow ventilation,
in addition, intensifies this process by creating turbulent (eddy) diffusion within the
burrow structures, and an advective transport of soluble contaminants over the
sediment-water interface (Thibodeaux et al. 2001).
Uptake in organisms Infauna are exposed to contaminants via several different routes, including pore
water and overlying water, as well as through the ingestion of contaminated
sediment particles. Generally, only truly dissolved contaminants can diffuse across
the cell membrane and the bioavailable fraction is consequently positively related to
the aqueous concentration of the compound (Landrum & Robbins 1990, Worms et
- 14 -
al. 2006). Uptake over the body surface or respiratory organs via interstitial or
overlying water therefore depends a lot on the partitioning properties of the
contaminant and the sediment OM content. For very hydrophobic (log Kow >6)
organic contaminants and many metals uptake via food is suggested to be the most
important route for deposit-feeding organisms (Leppänen & Kukkonen 1998,
Griscom et al. 2002). Dietary assimilation of contaminants by animals, however,
also assumes that the contaminant desorbs from the ingested material in the
digestive tract and is subsequently absorbed by the gut epithelium. Several factors
within the gut can influence the rate and extent of desorption, e.g. pH and
enzymatic activity of the digestive fluid, and contaminants that are not absorbed by
the organism are transported back to the sediment with the feces (Weston & Maruya
2002). Bioaccumulation is the net accumulation of a compound as a result of uptake
from all routes of exposure and loss from processes like metabolism and
elimination (Landrum et al. 1996). The simplest way to determine bioaccumulation
in infauna is to relate the steady state contaminant concentration in the animal to the
total concentration in the sediment and express it as a bioaccumulation factor, BAF.
This obviously does not explain any of the underlying mechanisms of
bioaccumulation and several models based on the understanding of contaminant
partitioning have been developed to increase the possibility to accurately predict
bioaccumulation. For HOCs, the equilibrium partitioning theory (EPT) assumes that
partitioning between the organism and the sediment is regulated by the organic
carbon content of the sediment, pore water concentration and lipid content of the
organism, which at equilibrium should result in a more or less constant biotasediment accumulation factor (BSAF) (Di Toro et al. 1991). Recently, much
attention has been given to the importance of also including the variability of
organic matter composition in these models (Cornelissen et al. 2005). The
partitioning and assimilation of metals is generally more complex than for HOCs
and other steady state models have been developed for metals, e.g. the free ion
activity model (FIAM) and the biotic ligand model (BLM), which include
environmental variables like dissolved OM, cation concentrations and pH (Niyogi
& Wood 2004, Luoma & Rainbow 2005).
Still, many models fail to accurately predict the bioaccumulation of contaminants
by deposit-feeding infauna. This highlights the importance of other factors, such as
- 15 -
the feeding ecology and physiology of the organisms, as well as the coupling
between their behavior and sediment biogeochemistry (cf. contaminant partitioning)
(Forbes & Forbes 1994, Leppänen & Kukkonen 2006). Most deposit-feeders are
selective feeders, choosing particles with high organic carbon content and nutritious
value (Jumars & Wheatcroft 1989). Moreover, accumulation depends on e.g. the
ingestion rate, digestive system and assimilation efficiency of the particular species
(Mayer et al. 1996). Uptake and bioaccumulation of contaminants by benthic
invertebrates can cause adverse effects, like behavioral changes, impaired
reproduction or death (Bombardier & Bermingham 1999). In this thesis, however,
bioaccumulation is not related to toxic effects but rather treated as a vector of
contaminants re-entering the ecosystem.
WHAT’S SO SPECIAL ABOUT THE BALTIC SEA? The semi-enclosed Baltic Sea is one of the world’s largest brackish water bodies
and is characterized by unique hydro-geographical and ecological features. It
consists of a series of basins separated by shallow sills and the average water depth
is ca. 60 m. A stable salinity gradient progresses from almost limnic conditions (2-3
psu) in the north to near marine (>20 psu) in the Danish Straits, where the Baltic
connects with the North Sea. The intrusions of dense saline water in the south and
the large riverine input of fresh water creates a halocline at 60-80 m in most of the
Baltic Sea (Matthäus & Schinke 1999). The water below the halocline is
permanently or periodically subjected to hypoxia/anoxia as a consequence of
infrequent saltwater intrusions, and the deep water residence time in the Baltic Sea
is more than 30 years (Meier et al. 2006). The brackish water Baltic Sea has a low
species diversity and functional complexity (Bonsdorff & Pearson 1999). The
Baltic biota consists of mainly euryhaline species originating from either marine or
freshwater environments. The macro-zoobenthic infauna is dominated by a few
species, primarily small-size shallow dwelling organisms (Laine 2003). The benthic
community structure has been described as being at an early successional stage
(Rumohr et al. 1996, Bonsdorff 2006), i.e. it is largely dominated by opportunistic,
stress-tolerant small organisms (Rosenberg 2001). For example, in the deeper soft
bottoms there is a lack of deep burrowing and subsurface deposit feeders
- 16 -
(Bonsdorff & Pearson 1999), and large taxonomic groups (such as echinoderms)
important in marine environments are totally absent from the southern Baltic Proper
and northwards (Elmgren 1984). As a consequence, the bioturbation mixing depth
in the Baltic Sea is generally shallow (<5 cm).
During the last 50 years, the Baltic Sea ecosystem has been under severe
anthropogenic stress, including hazardous chemicals, eutrophication and overfishing (Elmgren 2001). The Baltic Sea is enclosed by heavily industrialized
countries and more than 85 million people live within its drainage area. Although
monitoring indicates that the load of hazardous substances has been reduced
considerably over the past 20-30 years, problems persist (HELCOM 2008). For
example, the concentration of many contaminants in Baltic biota is high compared
to organisms in other marine environments (Berggren et al. 1999), several tons of
POPs and metals are stored in the Baltic sediments (Jonsson et al. 1990, Borg &
Jonsson 1996), and current levels of planar-PCBs and dioxins in many Baltic fish
species are exceeding the limit for human consumption set by the European Union
(Isosaari et al. 2006). The present-day main sources for some of these pollutants are
unclear, suggesting diffusive sources (Agrell et al. 2001). Although atmospheric
deposition probably is a major route of entry for new contaminants, another
potential source to the Baltic biota is remobilization from the large sediment
deposits and via food-web transfer from predation on infauna. Eutrophication in the
Baltic Sea has, as a secondary effect, led to an increased sedimentation rate of OM
and to decreased oxygen levels in benthic environments when the OM is
mineralized. Consequently, bottom areas with prevailing hypoxic/anoxic conditions
have been extended, particularly in deep areas below the halocline but also in
shallow coastal areas, leading to large-scale depletion of benthic infauna (Diaz &
Rosenberg 1995, Karlson et al. 2002). Recently, attention has been given to a
potentially new and increasing problem in the Baltic, i.e. the invasion of nonindigenous species (Leppäkoski et al. 2002). For example, the establishment of the
deep-burrowing (>35 cm) polychaete genus Marenzelleria has significantly
changed the benthic community structure in many areas (Zettler et al. 1995, Perus
& Bonsdorff 2004). However, the question remains as to whether it will have a
positive or negative effect on the Baltic Sea ecosystem.
- 17 -
METHODS AND STUDY ORGANISMS The sampling of sediment, water and organisms for all studies (except IV) in this
thesis was done in the southern Stockholm archipelago, NW Baltic Proper.
Monoporeia affinis and Macoma balthica were collected with a benthic sledge (>20
m; I-III), Marenzelleria sp. and Nereis diversicolor were sieved out on-site from
sandy sediment (1 m; I-III, V). Sediment for paper IV was collected in the inner
Stockholm Archipelago at 30 m depth and Marenzelleria neglecta in the DarssZingst Estuary, Germany.
Experimental systems All experiments were performed under controlled laboratory conditions using
acrylic tube core microcosms (8 cm Ø) with either sieved sediment (I-III, V) or
intact natural sediment cores collected from a ship and brought to the laboratory
(IV). In paper I, II and V the systems were kept static. In paper III and IV
individual water re-circulating systems were created, passing the overlying water
through a series of filters; i.e. first two glass fiber filters (GFs) for the collection of
particle-associated organic contaminants and then two polyurethane foam filters
(PUFs) in order to retain the soluble fraction (Fig 2). The physical resuspension in
paper III was generated by a motor-driven paddle, run twice a week.
Air in/out
Water
out
Water
in
Rotating
motor
Peristaltic
pump
PUF x2
1A)
GF/F
GF/D
1B)
Fig 2. Schematic figure of experimental units used paper III.
- 18 -
Contaminants, organic material and tracers The studied contaminants were either artificially added (spiked) radio-labeled
compounds (I-III) or ‘natural’ environmental pollutants present in the collected
sediment (IV). In paper I and II, the brominated flame retardant
(2,2’,4,4’,5-pentabromodiphenyl ether) and metal
14
C-BDE-99
109
Cd were added to the sediment
surface spiked to different types of organic matter (OM). In paper III, sediment was
spiked with a tri-chlorinated PCB,
14
C-PCB-32 (2,4',6-trichlorobiphenyl), and
added to each core as a 3 cm layer on top of underlying clean (un-spiked) sediment
(III). The advantages of using radio-labeled compounds are e.g. the possibility to
study the fate of a specific contaminant and to use concentrations well below
reported toxic levels due to high analytic detection capacity. It is also a relatively
cost- and time effective method compared to chemical analytical methods.
The different types of OM used in paper I and II were: 1) the microalgae
Tetraselmis spp., 2) kraft-lignin derived from terrestrial wood, and 3) surface
sediment. The different OM types represented a high (Tetraselmis), low (lignin) and
medium (sediment) quality OM source to the benthic invertebrates. The quality was
referred to as the nutritious value of the OM source, defined as the relative amount
of total nitrogen (TN) to total carbon (TC) in the OM, and the amount of amino
acids and fatty acids (Gunnarsson et al. 1999).
In paper V, inert particle (luminophores) and solute (Br-) tracers were added to each
core. Luminophores were added on the sediment surface, whereas bromide was
added to the overlying water column.
Study organisms The organisms used in this thesis were chosen based on their ecological importance
in the benthic communities of the Baltic Sea, as well as their functional differences
(Fig 3). The amphipod Monoporeia affinis and the bivalve Macoma balthica are
dominant members of the deeper soft sediments, both in terms of abundance and
biomass (Bonsdorff et al. 2003, Laine 2003). M. affinis is a surface deposit-feeder
mainly feeding on fresh organic matter (Byren et al. 2002). It burrows actively in
the upper few cm of the sediment and displays a nocturnal swimming behavior
(Lopez & Elmgren 1989, Lindström & Fortelius 2001). The clam M. balthica is less
- 19 -
motile, normally positioned ca. 5 cm into the sediment protruding its siphons to the
sediment surface, where it can switch between surface deposit- and suspensionfeeding (Olafsson 1986, Rumohr et al. 1996).
The invasion of the three sibling species of the polychaete genus Marenzelleria has
changed the community composition in many areas (Zettler et al. 2002, Perus &
Bonsdorff 2004). This spionid polychaete is a surface-deposit feeder, creating Jshaped semi-permanent burrows down to 35 cm (Zettler 1996). Apart from the
priapulid Halicryptus spinulosus, it is the only deep-burrowing species in the
northern Baltic Sea (Bonsdorff & Pearson 1999). They inhabit both shallow sandy
substrates as well as deeper more muddy sediments at abundances ranging from a
few hundred individuals per m2 up to 39 000 ind. per m2 (Kube et al. 1996). It is
very difficult to separate the sibling species by morphological identification. Based
on the results of Blank et al. (2008), who used genetic tools to identify and map the
species distribution in the Baltic Sea, it is most likely that the worms used in this
thesis were exclusively M. neglecta. In shallow coastal areas Marenzelleria spp. are
competing with the common ragworm Nereis (Hediste) diversicolor, that inhabits
sediments
down
to
ca
15
m
Monoporiea affinis
depth
(Rasmussen
1973).
Marenzelleria sp.
Macoma balthica
Nereis (Hediste) diversicolor
5 cm
10 cm
15 cm
Fig 3. Graphic illustration of the position in the sediment of species used in the thesis.
- 20 -
They
are
opportunistic omnivores, although their main feeding strategies are surface-deposit
and filter feeding (Scaps 2002). N. diversicolor lives in more or less permanent U or
Y-shaped burrows, creating a complex network of burrows extending down to ca.
15 cm that they are known to actively ventilate (Davey 1994).
In all experiments, the number of organisms added to the cores corresponded to
average field densities. Therefore, the density and biomass could differ between
treatments and all results relate to the natural field density of each species. This
choice was made to increase the ecological relevance of the studies to the field
situation.
Sampling and chemical analyses At the end of each experiment, the sediment was sectioned into ca. 1 cm slices and
organisms were carefully picked out by hand and placed in brackish water to let
them purge their gut before tissue residue analysis. In paper I-III, all samples were
analyzed using liquid scintillation counting (LSC) for the detection of
gamma spectrometry for
14
C and
109
Cd. Filters (GFs and PUFs) from experiments in III and
IV, as well as sediment and organisms in IV, were Soxhlet-extracted before
analysis. In paper III extracts were analyzed with LSC and in paper IV all extracts
were analyzed using a μ-electron capture detector capillary-gas-chromatograph
(GC-ECD), identifying 14 different organic contaminants (IV).
Luminophore analyses were done under UV-light followed by quantification using
image analysis software (V). Pore water bromide concentrations were determined
spectrophotometrically (Presley 1971). Luminophore profiles were fitted to a
gallery-diffusion model (Francois et al. 2002), quantifying the rate of particlemixing by giving two coefficients: an apparent biodiffusion coefficient, Db, and a
non-local transport coefficient, r.
- 21 -
PAPERS IN BRIEF ‐ RESULTS Fate of surface deposited contaminants Paper I and II: Interactive effects between bioturbation and settling OM BDE-99 and cadmium were deposited on the sediment surface associated with OM
of different nutritional qualities: phytoplankton, terrestrial lignin and sediment. The
burial, remobilization (I) and bioaccumulation (II) of the two contaminants by three
species with diverse feeding and bioturbation strategies, Monoporeia affinis,
Macoma balthica and Marenzelleria sp., were analyzed after 34 d.
Paper I: Fate There were clear species-specific differences and complex interactive effects
between the type of contaminant and OM. For example, the burial of BDE-99
generally decreased in the order Macoma balthica > Monoporeia affinis >
Marenzelleria, while the highest amount of Cd was buried by Marenzelleria. OM
type had no effect on the burial of BDE-99, but the addition of phytoplankton
significantly increased the burial of Cd by Marenzelleria. BDE-99 is highly
hydrophobic (log Kow >7) and sorbs strongly to particles and OM (de Wit 2002).
Cadmium, on the other hand, is probably less particle reactive and more mobile as a
dissolved chemical element. Results from paper I suggest that: 1) M. affinis and M.
balthica mix and bury particles and associated contaminants in a biodiffusive mode
while Marenzelleria does not cause any down-ward transport of particles, 2)
Marenzelleria can transport dissolved compounds in their burrow structures and
over the sediment-water interface by bio-irrigation, 3) bioturbation by all species
increase the retention of surface-deposited contaminants in the sediment, and 4)
OM type only seemed to be important as a sorbent, e.g. more Cd was released from
the labile OM (phytoplankton), and did not affect the intensity of particle and solute
mixing through bioturbation.
Paper II: Bioaccumulation OM quality significantly affected the bioaccumulation of both contaminants. For
Cd, bioaccumulation by all species was in the order Tetraselmis >> lignin >
sediment, while for BDE-99 the trend was Tetraselmis >> sediment ≥ lignin. The
normalization to sediment TOC and animal lipid (BSAF) for the accumulation of
- 22 -
BDE-99, did not remove the observed differences between treatments, thus
suggesting that other factors than simple partitioning were important. Hence, based
only on the nutritious quality of the OM, bioaccumulation was as hypothesized
highest when associated with the nutritious algae. Species-specific differences were
only significant for Cd, following Marenzelleria > Macoma > Monoporeia, but for
BDE-99 there were no general differences. The species-specific Cd accumulation
could be attributed to differences in the feeding ecology of the organisms, such as
feeding rate and particle selectivity. However, it may also be due to differences in
additional exposure routes, i.e. uptake of dissolved Cd from pore water and
overlying water, particularly for Marenzelleria sp. that was shown to transport Cd
via bio-irrigation (I). Due to the high Kow of BDE-99, the primary route of exposure
to the organisms was probably through the diet.
Remobilization of sediment‐associated contaminants Paper III: Comparing bioturbation and physical resuspension Physical processes are generally considered more important than biological in the
remobilization of sediment-associated contaminants. Two modes of bioturbationdriven release of PCB (biodiffusion by Monoporeia affinis and bio-irrigation by
Marenzelleria sp.) were compared to the release due to physical sediment
resuspension generated by a motor-driven paddle, aiming at simulating the transient
and episodic events that are likely to occur in the deeper accumulation areas of the
Baltic Sea. Fluxes of soluble and particle-associated PCB-32 (log Kow 5.4) were
quantified weekly during 30 days. Both bioturbation and physical resuspension
significantly increased the PCB fluxes compared to controls. The relative
importance of remobilized dissolved vs. particle-associated PCB differed between
treatments, suggesting differences in the driving mechanisms behind the flux.
Bioturbation by M. affinis caused the highest flux of both PCB fractions compared
to the other treatments, while Marenzelleria sp. only remobilized dissolved PCB.
This could be related to their specific modes of bioturbation; amphipods actively
mix the upper sediment layer as well as suspend sediment particles, and the
polychaetes create and irrigate semi-permanent burrows. The physical disturbance
resulted in a very high concentration of suspended particles in the water column
immediately after each resuspension event (every 3-4 days), however, over the
- 23 -
whole experiment time the total flux of particles, and particle-associated PCB, was
still lower than the flux caused by the continuous bioturbation by Monoporeia
affinis. There was little difference in the flux of dissolved PCB caused by
Marenzelleria sp. (1.7 times higher than controls) and by physical resuspension (2.1
times higher). In all treatments, the release of dissolved PCB was more than an
order of magnitude higher than that of particle-associated PCB, indicating a
significant potential exposure route to pelagic organisms of the most bioavailable
PCB form. Calculated mass transfer coefficients (0.43-1.37 cm d-1) corresponded to
previously reported values for tri-chlorinated PCBs. Results in paper III indicate
that the continuous activities of benthic infauna can be just as, or even more,
important than the large, but intermittent, pulses of physically resuspended
sediment for the remobilization of sediment-bound contaminants.
Paper IV: The effect of oxygenation and recolonisation of laminated sediments Extended periods of anoxic/hypoxic conditions in bottom waters of the Baltic Sea
have led to depletion of bioturbating macrofauna and subsequent spreading of
laminated sediments, and it has been estimated that up to 30 tons of PCBs may be
stored in these sediments. In paper IV, the effects of reoxygenation and subsequent
bioturbation on the release of POPs from naturally contaminated and laminated
Baltic Sea sediments were investigated. The sediment was bioturbated by the
invasive polychaete Marenzelleria neglecta, that is tolerant to low oxygen levels
and can potentially rapidly colonize areas after periodic anoxia/hypoxia. The flux of
both soluble and particle-associated POPs from sediment to water, including HCHs,
HCB, DDTs and PCBs, was quantified after 85 days. Oxygenation followed by
bioturbation by M. neglecta significantly increased the flux of dissolved POPs (0.73 times) compared to hypoxic sediments but had no effect on the remobilization of
particle-associated POPs. Only oxygenation slightly decreased the flux of POPs
perhaps as a result of co-precipitation of DOM-associated POPs and ferrous oxides
following aeration. As in paper III, the flux of dissolved PCB always exceeded the
B
flux of particle-associated PCB by an order of magnitude. MTCs (Kf) were between
0.06-0.45 and 0.1-1.8 cm d-1 in the oxygenated only and bioturbated cores,
respectively. There was a positive correlation between Kf and log Kow, explaining
75% of the variation in the oxygenated cores but only 44% in the bioturbated cores,
suggesting that other factors than hydrophobicity regulated the soluble release of
- 24 -
contaminants from the bioturbated sediments, i.e. likely the creation and bioirrigation of burrows exposing contaminants at depth. Colonization of laminated
sediments by M. neglecta could generate a substantial release of bioavailable POPs
from sediment to water.
Bioturbation mechanisms Paper V: Particle and solute transport by two polychaetes The effects of bioturbation on sediment biogeochemistry have been shown to be
highly species-specific, and can be linked to particular feeding and burrowing
strategies. It is therefore of interest to characterize and quantify the bioturbation
efficiency of individual species for a better prediction and understanding of
processes such as cycling of nutrients and contaminants in the sediment
compartment. Paper V investigated the particle-mixing and solute transport by
Marenzelleria sp. and Nereis diversicolor in Baltic Sea sediments using inert
particle (luminophores) and solute (Br-) tracers. To quantify the intensity of particle
reworking, a gallery-diffusion model was used to calculate the biodiffusion
coefficient, Db, and non-local transport parameter, r. A higher percentage of
luminophores was buried below the top 0.5 cm surface layer by Nereis (13%) than
by Marenzelleria (6%), as well as to a greater depth (5 vs. 1.5 cm). Db did not
differ between the two worms (2.4 x 10-3 cm2 d-1) indicating a similar mixing rate of
the top 1-2 cm sediment. On the other hand, the model only detected non-local
transport by Nereis (r: 2.5 y-1). Thus, results suggest that Nereis is a more efficient
particle-reworker than Marenzelleria. Bioturbation by both worms significantly
increased the sediment pore water Br- concentrations compared to controls. The
shape of the bromide profiles in the Marenzelleria cores indicated that the worms
caused an enhanced diffusion (biodiffusion) in the upper 1-1.5 cm followed by an
advective transport down to ca. 8 cm. In Nereis the bromide profiles were more
varied but generally showed an enhanced diffusion throughout the whole core with
sub-surface peaks. Compared to controls, Marenzelleria increased the net flux of
bromide into the sediment 4-6 times and Nereis 3-5 times. The two polychaete
worms displayed different modes and intensity of bioturbation, which adds
information to the understanding of how the invasion of Marenzelleria can affect
important benthic processes in the Baltic Sea.
- 25 -
DISCUSSION Bioturbation and the fate of contaminants in the Baltic Sea The three infaunal species studied in paper I-IV displayed distinctly different
modes of bioturbation and had significantly different effects on the burial and
remobilization of contaminants. The active particle mixing of the upper 2-3 cm of
the sediment by the amphipod Monoporeia affinis resulted in both increased burial
and retention of surface deposited contaminants in the sediment (I), as well as an
enhanced release of sediment-bound PCB from sediment to water (III). They
caused substantial water column turbidity by bioresuspenion of sediment particles
(I, III) and thus also particle-associated contaminants (III). The clam Macoma
balthica is less motile than M. affinis but can also be categorized as a biodiffuser
(Bradshaw et al. 2006, I). Their main effect on the sediment contaminant
distribution is probably by passive transport of particle-associated contaminants as a
result of particles falling into the space created around their shells when they move
around (I). The clams caused little particle resuspension, in fact suspension-feeding
may instead filter out both suspended particles and contaminants present in the
water and increase the deposition of contaminants on the sediment surface through
biodeposition (Gilek et al. 1997, I). Bivalves have been found to have limited
effects on contaminant fate (Riedel et al. 1997, I) compared to other groups of
infauna (e.g. polychaetes), probably due to generally lower motility and lack of bioirrigation. The polychaete Marenzelleria sp. also appeared to have a low motility,
largely remaining in their burrows except when venturing out searching for food
around their burrow entrance. They did not cause any significant particle mixing
below the top surface layer (<0.5 cm), although a localized transport within their
burrow structures was indicated (I, V). On the contrary, the worms were effective
bio-irrigators (V). The most important effect on contaminant transport by
Marenzelleria sp. is thus via bio-irrigation, thereby primarily influencing the fate of
dissolved and/or DOM-associated contaminants (I-IV).
Infauna are often not considered important when studying the large-scale fate of
contaminants and the main focus is usually on physical processes (Jonsson 2000).
However, on a local scale, the activities of benthic invertebrates can both enhance
(Ciutat et al. 2006) and even exceed (Riedel et al. 1987, III) the effects of physical
- 26 -
processes for contaminant transport. The bottom current and wave induced physical
disturbance of the sediment in the deeper accumulation areas of the Baltic Sea is
generally weak and sporadic (Stips et al. 1998, Danielsson et al. 2007). Compared
to the continuous process of biologically mediated sediment resuspension, periodic
and short-lived physical resuspension swiftly entrain a lot of particles that rapidly
re-settle back on to the sediment surface, suggesting that over time bioresuspension
can dominate the particle flux in these environments. Results in paper III support
this assumption, showing that bioturbation by Monoporeia affinis caused a higher
flux of particles and particle-associated PCB from sediment to water than simulated
physical resuspension. The release of dissolved PCB after physical resuspension is
probably mainly due to desorption from resuspended particles and a rapid release of
surface pore water (Schneider et al. 2007). Despite a lack of particle resuspension
by Marenzelleria sp., bioturbation by the worm and physical resuspension caused a
similar flux of dissolved PCB to the water, showing the importance of a slower but
continuous advective transport via bio-irrigation (III). The relative effects of
physical vs. biological disturbance for the fate of contaminants is clearly dependent
on the specific hydrographic, geochemical, and biological properties of the benthic
system, as well as the physiochemical properties of the contaminant. Results
presented here suggest that bioturbation by common Baltic invertebrates affects
contaminant fate in the benthic environment in a species-specific way, both
increasing the retention and enhancing remobilization, and that it can be just as, or
even more, important than physical resuspension for the remobilization of
sediment-bound contaminants.
The multiple roles of organic matter for contaminant fate Settling organic matter (OM) is the main food source for deposit feeding infauna
below the photic zone and the supply typically varies in time, quantity and quality.
Moreover, OM is one of the most important sorbents for HOCs and metals and
contaminants thus often reach the sediment associated to OM of various origins.
Ingestion of contaminated food-particles is an important route of exposure for
deposit-feeding infauna and it has been shown that bioaccumulation of HOCs
(Gunnarsson et al. 1999) and metals (Maloney 1996) can be correlated to the
nutritious value of the sediment OM. The bioaccumulation of BDE-99 and
cadmium by Baltic infauna was significantly higher when associated to a labile
- 27 -
microalgae, simulating the deposition of contaminants to the benthic system with a
settling phytoplankton bloom, compared to when associated with lignin (cf.
terrestrial run-off) or sediment (cf. sediment resuspension) (II). This result was
probably largely due to selective feeding by the organisms and a higher feeding rate
in the algae treatment, although differences in sorption capacity of the various OM
types also needs to be considered. For example, contaminants were likely more
readily desorbed from the labile algae than the lignin or sediment, which increased
the animals’ exposure from dissolved compounds in the pore water. This was
supported by the concurrent higher bioaccumulation and transport of soluble
cadmium in the algae treatment by Marenzelleria sp. compared to the other species
(I, II). Therefore, there are likely seasonal differences in the bioaccumulation and
transport of contaminants in the Baltic benthic ecosystem as well as differences
depending on community composition (Gunnarsson et al. 2000, I, II).
Eutrophication has increased the load of sinking OM in the Baltic Sea and the
bottom areas suffering from hypoxic/anoxic bottom water conditions and depletion
of benthic macrofauna has increased as a result (Karlson et al. 2002). Several
actions are currently being taken by countries around the Baltic Sea to reduce the
input of nutrients and decrease eutrophication (Backer & Leppänen 2008). The
recolonisation of these sediments following improved oxygen conditions could lead
to a significant increase in the release of contaminants (IV). A colonization
dominated by the opportunistic and low-oxygen tolerant Marenzelleria spp.
(Hahlbeck et al. 2000) would not result in a general mixing of the sediment but
rather an enhanced diffusive flux of dissolved contaminants from the sediment to
the water (I, III-V). The establishment of Marenzelleria spp. can enhance the
overall sediment redox condition and allow subsequent colonization by other less
tolerant species, like Monoporeia affinis. Results from paper I-III highlighted the
importance of understanding the complex interactions between ecological (e.g.
infaunal feeding and bioturbation, OM cycling) and physicochemical processes
(e.g. contaminant partitioning) when assessing the fate of contaminants in a
sediment ecosystem.
- 28 -
Potential effects of the invasion of Marenzelleria Since their invasion in the 1980s, the polychaete genus Marenzelleria has
completely changed the benthic community structure and they are now the
dominant species in many areas (Perus & Bonsdorff 2004). The previously
abundant Monoporeia affinis has concomitantly decreased (Perus & Bonsdorff
2004), and although there are indications of inter-specific competition between the
two species (Kotta & Olafsson 2003) the exact reasons behind the decline of the
amphipod populations are not fully understood (Jacobson 2008). Based on results
presented in this thesis, a shift from a community dominated by M. affinis/ Macoma
balthica to one dominated by Marenzelleria spp. could affect the contaminant fate
in different ways depending on the type of contaminant and the specific situation.
Bioturbation by Monoporeia/Macoma contribute to the incorporation of ‘new’
contaminants, deposited on the sediment surface or from the water column, into the
sediment, which will enhance the retention and thus decrease the risk of
remobilization. On the other hand, particle-mixing and altering effects on the
sediment biogeochemistry, in particular by Monoporeia, also result in the release of
sediment-bound contaminants back to the water column. In areas with on-going
pollution and high contaminant concentrations in the sediment surface layer, this
could probably cause a rapid recycling of contaminants between the sediment and
the overlying water. However, reduced inputs of many POPs and metals during the
last decades has resulted in a gradual decrease of contaminant concentrations in the
upper sediment layers in most areas, and the vertical distribution of many POPs and
metals typically shows a sub-surface peak below 5 cm, i.e. below the maximum
burial depth of most native species in deep soft-bottoms. Marenzelleria, however,
can reach these deposits through their creation of deep burrows (>35 cm) and thus
significantly increase the remobilization of historical contaminants. In addition,
Marenzelleria does not contribute to the burial and retention of new surface
deposited contaminants, although they might increase the incorporation of soluble
contaminants via irrigation. Ecological studies on the effects of the invasion by
Marenzelleria spp. are inconclusive (Orlova et al. 2006); it is clear that the benthic
community structure has changed but whether this is positive (increased
biodiversity, functional complexity) or negative (inter-specific competition,
enhanced recycling of contaminants and nutrients) for the Baltic Sea ecosystem
remains unclear.
- 29 -
CONCLUSIONS Long-term environmental monitoring studies show a significant decline of
contaminants in Baltic biota (Bignert et al. 1998). Apart from successful source
control and reduced environmental input, this might suggest little or no
remobilization of historic contaminants from the large sediment deposits. No
bioturbation in the widespread anoxic/hypoxic bottom areas and weak physical
forcing in the deep accumulation basins potentially make these sediments efficient
traps of contaminants. However, improved benthic redox conditions and
recolonisation by sediment-living organisms could instead turn the sediments from
a sink into a source. This issue is of particular concern when combined with the
invasion of Marenzelleria spp., since these worms can burrow deep into the
sediment to remobilize historic deposits. In addition, declining loads of
contaminants to the Baltic Sea increase the relative importance of sediments as
secondary sources to the ecosystem. In summary, bioturbation is an important
process influencing the fate of contaminants in the Baltic Sea benthic system and its
importance may increase with the invasion of new deeper-digging species. Such
new additions to the Baltic fauna can lead to changes in functional diversity
(bioturbation mode and depth) as well as the food-web structure (additional prey
items) that could alter the pathways and distribution of contaminants in the Baltic
Sea ecosystem.
- 30 -
ACKNOWLEDGEMENTS Doing a PhD is a life experience and, as most other things in life, cannot be done
without a little help (or a lot) from your friends. This work has been completed with
the support from many people and to all of you: Thank you!
Before meeting my supervisor Jonas Gunnarsson, I did not know that mud could be
described in so many words and with such passion, I did not know that sediment
ecotoxicology without doubt was the most interesting field of research, and I did
not know that worms make the world turn. I have learnt a lot. Jonas, you have
shown that dedication and enthusiasm will take you a long way. It has been
inspiring to work with you, thank you for all your knowledge and support! My cosupervisor Nils Kautsky, thank you for always keeping it real!
A big big thank you to all my co-authors! Maria T, without all the frozen talks and
laughter in the cold room I would not have made it through the first years. Clare,
the eye of the storm, many thanks for good company in the lab, lots of scientific
input and proof readings (and nice dinners). Micke G, I really appreciate your time
for discussions and all your support throughout this period. Mia G, you are always a
step ahead of me and an inspiration to go forward, thank you for all your input!
I have also had the opportunity to collaborate and exchange knowledge with many
other bright scientists. In particular, I would like to thank Franck Gilbert for
welcoming me to Marseille and trying to make me understand the world of models,
not easy! To Gary Banta, thank you for inviting me to work in your lab, I really
enjoyed working with you and Anne and getting to know many others at RUC. We
still have some unfinished business but that only gives me a good reason to
continue working with you! Others that have given a lot of help and support are
Mats and Olivia at KTH, Ulla, Lillemor, Brita and Marie at ITM, Rasmus the
Marenzelleria-expert, Kerstin G and Linda K at the Department, Master’s students
Cecilia and Julia and all other students giving inspiration over the years. I also want
to thank Anders S and his lab for all their help.
- 31 -
To all friends and colleagues at the Department of Systems Ecology: thank you for
creating a fun and relaxed atmosphere to work in! In particular, my salute goes to
the Ecotox-group, past and present office-mates Marc, Sigrid, Johan N, Angelina
and Micaela, the mud people Johan N, Agnes and Francisco, innebandy/
climbing/beer friends Micke T, Johanna, Johan E, Lisa A, Gustaf A, Alma, Albert,
Jerker and many more! And, of course, without Lasse, Barbara and Siw the
Department would not function.
Many things have also happened outside work during this PhD. Some of the best
things have happened while standing on my head! The world of acrobatics just hit
me like a club and I have met some of the finest and funniest friends one could ever
wish for: Marie, Niklas, Tim, James, Tove & Andreas, Camilla & Anthony, Tomas,
Karin and the rest of the crew – hep, I love you all! A big kiss to Ammi, Anna,
Alfred and Mr. Jazz Pierre, we all started on the same spot in Umeå and have ended
up in Stockholm (-ish) despite taking very different trails. I am so happy you are
here! Carro, my homie – never longer than a phone call away, you are very dear to
me. Thank you and the family for always feeding me with what I need! So close
and yet so far away – Frøydis, I miss you here. You bring cheerfulness,
encouragement, comfort and challenges. And you are a kick-ass illustrator! Thank
you for always standing by me, I look forward to see you, T, e and xxx soon again.
Tante grazie per tutta la famiglia Buemi-Sacco, che ogni anno mi ha dato gioia, sole
e cibo superiore! Marco (trask), no one has waited longer than you, I am so happy
you are still beside me to share this day. Baci!
Most of all my thanks go to my wonderful family! Kristian and Lenita, thank you
for all support, now I hope to see more of my two favorite little people in the world!
Cecilia, friend and sister, thank you and Erik for always making me feel welcome in
your home. Finally – mamma och pappa – for never ending love, support and joy, I
dedicate this thesis to you.
- 32 -
REFERENCES Agrell C, Larsson P, Okla L, Bremle G, Johansson N, Klavins M, Roots O, Zelechowska A (2001)
Atmospheric and river input of PCBs, DDTs and HCHs to the Baltic Sea. In: Wulff F (ed)
Ecological Studies, Vol 148. Springer-Verlag, p 149-174
Allen-King RM, Grathwohl P, Ball WP (2002) New modeling paradigms for the sorption of hydrophobic
organic chemicals to heterogeneous carbonaceous matter in soils, sediments, and rocks.
Advances in Water Resources 25:985-1016
Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediment and overlying
water. In: PL McCall and MJS Tevesz (eds). Animal-sediment relations. The biogenic
alteration of sediments. Plenum Press, NY, p 53-102
Aller RC, Aller JY (1998) The effect of biogenic irrigation intensity and solute exchange on diagenetic
reaction rates in marine sediments. Journal of Marine Research 56:905-936
Backer H, Leppänen JM (2008) The HELCOM system of a vision, strategic goals and ecological
objectives: implementing an ecosystem approach to the management of human activities in
the Baltic Sea. Aquatic Conservation-Marine and Freshwater Ecosystems 18:321-334
Baker JE, Eisenreich SJ, Johnson TC, Halfman BM (1985) Chlorinated-Hydrocarbon Cycling in the
Benthic Nepheloid Layer of Lake-Superior. Environmental Science & Technology 19:854861
Berggren P, Ishaq R, Zebuhr Y, Näf C, Bandh C, Broman D (1999) Patterns and levels of
organochlorines (DDTs, PCBs, non-ortho PCBs and PCDD/Fs) in male harbour porpoises
(Phocoena phocoena) from the Baltic Sea, the Kattegat-Skagerrak Seas and the west coast of
Norway. Marine Pollution Bulletin 38:1070-1084
Bignert A, Olsson M, Persson W, Jensen S, Zakrisson S, Litzen K, Eriksson U, Haggberg L, Alsberg T
(1998) Temporal trends of organochlorines in Northern Europe, 1967-1995. Relation to
global fractionation, leakage from sediments and international measures. Environmental
Pollution 99:177-198
Blank M, Laine AO, Juerss K, Bastrop R (2008) Molecular identification key based on PCR/RFLP for
three polychaete sibling species of the genus Marenzelleria, and the species' current
distribution in the Baltic Sea. Helgoland Marine Research 62:129-141
Bombardier M, Bermingham N (1999) The SED-TOX index: Toxicity-directed management tool to
assess and rank sediments based on their hazard - Concept and application. Environmental
Toxicology & Chemistry 18:685-698
Bonsdorff E (2006) Zoobenthic diversity-gradients in the Baltic Sea: Continuous post-glacial succession
in a stressed ecosystem. Journal of Experimental Marine Biology and Ecology 330:383-391
Bonsdorff E, Laine AO, Hänninen JH, Vuorinen I, Norkko A (2003) Zoobenthos of the outer
archipelago waters (N. Baltic Sea) - the importance of local conditions for spatial distribution
patterns. Boreal Environment Research 8:135-145
Bonsdorff E, Pearson TH (1999) Variation in the sublittoral macrozoobenthos of the Baltic Sea along
environmental gradients: A functional-group approach. Australian Journal of Ecology
24:312-326
Borg H, Jonsson P (1996) Large-scale metal distribution in Baltic Sea sediments. Marine Pollution
Bulletin 32:8-21
Boudreau BP (2001) Solute transport above the sediment-water interface. In: BP Boudreau and BB
Jørgensen (eds) The Benthic Boundary Layer. Oxford University Press, Inc., New York, p
104-123
Bradshaw C, Kumblad L, Fagrell A (2006) The use of tracers to evaluate the importance of bioturbation
in remobilising contaminants in Baltic sediments. Estuarine Coastal and Shelf Science
66:123-134
Byren L, Ejdung G, Elmgren R (2002) Comparing rate and depth of feeding in benthic deposit-feeders: a
test on two amphipods, Monoporeia affinis (Lindstrom) and Pontoporeia femorata Kroyer.
Journal of Experimental Marine Biology and Ecology 281:109-121
Chapman PM, Wang FY, Janssen C, Persoone G, Allen HE (1998) Ecotoxicology of metals in aquatic
sediments: binding and release, bioavailability, risk assessment, and remediation. Canadian
Journal of Fisheries and Aquatic Sciences 55:2221-2243
Chou SFJ, Griffin RA (1986) Solubility and soil mobility of polychlorinated biphenyls. In: JS Waid (ed)
PCBs and the environment, Vol 1. CRC Press inc., Boca Raton, Florida, p 101-120
- 33 -
Ciarelli S, van Straalen NM, Klap VA, van Wezel AP (1999) Effects of sediment bioturbation by the
estuarine amphipod Corophium volutator on fluoranthene resuspension and transfer into the
mussel (Mytilus edulis). Environmental Toxicology & Chemistry 18:318-328
Ciutat A, Widdows J, Readman JW (2006) Influence of cockle Cerastoderma edule bioturbation and
tidal-current cycles on resuspension of sediment and polycyclic aromatic hydrocarbons.
Marine Ecology-Progress Series 328:51-64
Cornelissen G, Gustafsson O, Bucheli TD, Jonker MTO, Koelmans AA, Van Noort PCM (2005)
Extensive sorption of organic compounds to black carbon, coal, and kerogen in sediments and
soils: Mechanisms and consequences for distribution, bioaccumulation, and biodegradation.
Environmental Science & Technology 39:6881-6895
Danielsson A, Jonsson A, Rahm L (2007) Resuspension patterns in the Baltic proper. Journal of Sea
Research 57:257-269
Davey JT (1994) The architecture of burrow of Nereis diversicolor and its quantification in relation to
sediment- water exchange. Journal of Experimental Marine Biology and Ecology 179:115129
de Wit CA (2002) An overview of brominated flame retardants in the environment. Chemosphere
46:583-624
Diaz R, Rosenberg R (1995) Marine benthic hypoxia - review of ecological effects and behavioral
responses of benthic macrofauna. Oceanogr. Mar. Ecol. Ann. Rev. 33:245-303
Di Toro DM, Mahony JD, Hansen DJ, Scott KJ, Hicks MB, Mayr SM, Redmond MS (1990) Toxicity of
cadmium in sediments: The role of acid volatile sulfide. Environmental Toxicology &
Chemistry 9:1487-1502
Di Toro DM, Zarba CS, Hansen DJ, Berry WJ, Swartz RC, Cowan CE, Pavlou SP, Allen HE, Thomas
NA, Paquin PR (1991) Technical Basis for Establishing Sediment Quality Criteria for
Nonionic Organic-Chemicals Using Equilibrium Partitioning. Environmental Toxicology &
Chemistry 10:1541-1583
Eggleton J, Thomas KV (2004) A review of factors affecting the release and bioavailability of
contaminants during sediment disturbance events. Environment International 30:973-980
Elmgren R (1984) Trophic dynamics in the enclosed, brackish Baltic Sea. Rapports et Procés-verbaux
des Réunions. Conseil International pour l’Éxploration de la Mer 183:152-169
Elmgren R (2001) Understanding human impact on the Baltic ecosystem: Changing views in recent
decades. Ambio 30:222-231
Erickson MJ, Turner CL, Thibodeaux LJ (2005) Field observation and modeling of dissolved fraction
sediment-water exchange coefficients for PCBs in the Hudson River. Environmental Science
& Technology 39:549-556
Forbes VE, Forbes TL (1994) Integrated ecotoxicology: linking fate and effect within a biological
hierarchy. In: MH Depledge and B Sanders (eds) Ecotoxicology in theory and practice.
Chapman & Hall, London, Glasgow, New York, Tokyo, Melbourne, Madras, p 149-183
Francois F, Gerino M, Stora G, Durbec JP, Poggiale JC (2002) Functional approach to sediment
reworking by gallery-forming macrobenthic organisms: modeling and application with the
polychaete Nereis diversicolor. Marine Ecology-Progress Series 229:127-136
Gerino M, Stora G, Francois-Carcaillet F, Gilbert F, Poggiale JC, Mermillod-Blondin F, Desrosiers G,
Vervier P (2003) Macro-invertebrate functional groups in freshwater and marine sediments:
A common mechanistic classification. Vie Et Milieu-Life and Environment 53:221-231
Gilek M, Björk M, Broman D, Kautsky N, Kautsky U, Näf C (1997) The role of the blue mussel, Mytilus
edulis, in the cycling of hydrophobic organic contaminants in the Baltic proper. Ambio
26:202-209
Gong YY, Depinto JV, Rhee GY, Liu X (1998) Desorption rates of two PCB congeners from suspended
sediments - I. Experimental results. Water Research 32:2507-2517
Grathwohl P (1990) Influence of organic-matter from soils and sediments from various origins on the
sorption of some chlorinated aliphatic-hydrocarbons - Implications on Koc correlations.
Environmental Science & Technology 24:1687-1693
Griscom SB, Fisher NS, Luoma SN (2002) Kinetic modeling of Ag, Cd and Co bioaccumulation in the
clam Macoma balthica: quantifying dietary and dissolved sources. Marine Ecology-Progress
Series 240:127-141
Gunnarsson J, Björk M, Gilek M, Granberg M, Rosenberg R (2000) Effects of eutrophication on
contaminant cycling in marine benthic systems. Ambio 29:252-259
- 34 -
Gunnarsson JS, Granberg ME, Nilsson HC, Rosenberg R, Hellman B (1999) Influence of sedimentorganic matter quality on growth and polychlorobiphenyl bioavailability in echinodermata
(Amphiura filiformis). Environmental Toxicology & Chemistry 18:1534-1543
Hahlbeck E, Arndt C, Schiedek D (2000) Sulphide detoxification in Hediste diversicolor and
Marenzelleria viridis, two dominant polychaete worms within the shallow coastal waters of
the southern Baltic Sea. Comparative Biochemistry and Physiology B-Biochemistry &
Molecular Biology 125:457-471
Heilskov AC, Holmer M (2003) Influence of benthic fauna on organic matter decomposition in organicenriched fish farm sediments. Vie Et Milieu-Life and Environment 53:153-161
HELCOM – Helsinki Commission, Baltic Marine Environment Protection Commission. www.helcom.fi.
October 2008.
Huang WL, Ping PA, Yu ZQ, Fu HM (2003) Effects of organic matter heterogeneity on sorption and
desorption of organic contaminants by soils and sediments. Applied Geochemistry 18:955972
Huettel M, Gust G (1992) Impact of bioroughness on interfacial solute exchange in permeable
sediments. Marine Ecology-Progress Series 89:253-267
Isosaari P, Hallikainen A, Kiviranta H, Vuorinen PJ, Parmanne R, Koistinen J, Vartiainen T (2006)
Polychlorinated dibenzo-p-dioxins, dibenzofurans, biphenyls, naphthalenes and
polybrominated diphenyl ethers in the edible fish caught from the Baltic Sea and lakes in
Finland. Environmental Pollution 141:213-225
Jacobson T, Prevodnik, A., Sundelin, B. (2008) Combined effects of temperature and a pesticide on the
Baltic amphipod Monoporeia affinis. Aquatic Biology 1:269-276
Jonsson P (2000) Sediment burial of PCBs in the offshore Baltic Sea. Ambio 29:260-267
Jonsson P, Carman R, Wulff F (1990) Laminated sediments in the Baltic - a tool for evaluating nutrient
mass balances. Ambio 19:152-158
Jumars PA, Wheatcroft RA (1989) Responses of benthos to changing food quality and quantity, with a
focus on deposit feeding and bioturbation. In: WH Berger, VS Smetacek, G Wefer (eds)
Productivity in the ocean: present and past. John Wiley & Sons Limited, p 235-253
Karickhoff SW, Brown DS, Scott TA (1979) Sorption of hydrophobic pollutants on natural sediments.
Water Research 13:241-248
Karlson K, Rosenberg R, Bonsdorff E (2002) Temporal and spatial large-scale effects of eutrophication
and oxygen deficiency on benthic fauna in Scandinavian and Baltic waters - A review. In:
Oceanography and Marine Biology, Vol 40, TAYLOR & FRANCIS LTD, London, p 427489
Ko FC, Sanford LP, Baker JE (2003) Internal recycling of particle reactive organic chemicals in the
Chesapeake Bay water column. Marine Chemistry 81:163-176
Kotta J, Olafsson E (2003) Competition for food between the introduced polychaete Marenzelleria
viridis (Verrill) and the native amphipod Monoporeia affinis Lindström in the Baltic Sea.
Journal of Sea Research 50:27-35
Kristensen E, Andersen FO, Blackburn TH (1992) Effects of benthic macrofauna and temperature on
degradation of macroalgal detritus - the fate of organic-carbon. Limnology and Oceanography
37:1404-1419
Kube J, Zettler ML, Gosselck F, Ossig S, Powilleit M (1996) Distribution of Marenzellaria viridis
(polychaeta: spionidae) in the South Western Baltic Sea in 1993/94 - Ten years after
introduction. Sarsia 81:131-142
Laine AO (2003) Distribution of soft-bottom macrofauna in the deep open Baltic Sea in relation to
environmental variability. Estuarine Coastal and Shelf Science 57:87-97
Landrum PF, Harkey GA, Kukkonen J (1996) Evaluation of organic contaminant exposure in aquatic
organisms: The significance of bioconcentration and bioaccumulation. In: MC Newman and
CH Jagoe (eds) Ecotoxicology a hierarchical treatment. Lewis Publishers, Boca Raton,
Florida, p 85-131
Landrum PF, Robbins JA (1990) Bioavailability of sediment-associated contaminants to benthic
invertebrates. In: R Baudo, JP Giesy and H Muntau (eds) Sediments: Chemistry and toxicity
of in-place pollutants. Lewis publishers, Ann Arbor, Boca Raton, Boston, p 237-263
Leppäkoski E, Gollasch S, Gruszka P, Ojaveer H, Olenin S, Panov V (2002) The Baltic - a sea of
invaders. Canadian Journal of Fisheries and Aquatic Sciences 59:1175-1188
Leppänen MT, Kukkonen JVK (1998) Relative importance of ingested sediment and pore water as
bioaccumulation routes for pyrene to oligochaete (Lumbriculus variegatus, Muller).
Environmental Science & Technology 32:1503-1508
- 35 -
Leppänen MT, Kukkonen JVK (2006) Evaluating the role of desorption in bioavailability of sedimentassociated contaminants using oligochaetes, semipermeable membrane devices and Tenax
extraction. Environmental Pollution 140:150-163
Lindström M, Fortelius W (2001) Swimming behaviour in Monoporeia affinis (Crustacea : Amphipoda)
- dependence on temperature and population density. Journal of Experimental Marine
Biology and Ecology 256:73-83
Lopez G, Elmgren R (1989) Feeding depths and organic absorption for the deposit-feeding benthic
amphipods Pontoporeia affinis and Pontoporeia femorata. Limnology and Oceanography
34:982-991
Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying
concept. Environmental Science & Technology 39:1921-1931
Maloney J (1996) Influence of organic enrichment on the partitioning and bioavailability of cadmium in
a microcosm study. Marine Ecology-Progress Series 144:147-161
Matthäus W, Schinke H (1999) The influence of river runoff on deep water conditions of the Baltic Sea.
Hydrobiologia 393:1-10
Mayer LM, Chen Z, Findlay RH, Fang JS, Sampson S, Self RFL, Jumars PA, Quetel C, Donard OFX
(1996) Bioavailability of sedimentary contaminants subject to deposit-feeder digestion.
Environmental Science & Technology 30:2641-2645
Meier HEM, Feistel R, Piechura J, Arneborg L, Burchard H, Fiekas V, Golenko N, Kuzmina N,
Mohrholz V, Nohr C, Paka VT, Sellschopp J, Stips A, Zhurbas V (2006) Ventilation of the
Baltic Sea deep water: A brief review of present knowledge from observations and models.
Oceanologia 48:133-164
Morse JW, Luther GW (1999) Chemical influences on trace metal-sulfide interactions in anoxic
sediments. Geochimica Et Cosmochimica Acta 63:3373-3378
Niyogi S, Wood CM (2004) Biotic ligand model, a flexible tool for developing site-specific water
quality guidelines for metals. Environmental Science & Technology 38:6177-6192
Olafsson EB (1986) Density dependence in suspension-feeding and deposit-feeding populations of the
bivalve Macoma balthica: A field experiment. The Journal of Animal Ecology 55:517-526
Orlova MI, Telesh IV, Berezina NA, Antsulevich AE, Maximov AA, Litvinchuk LF (2006) Effects of
nonindigenous species on diversity and community functioning in the eastern Gulf of Finland
(Baltic Sea). Helgoland Marine Research 60:98-105
Ortiz E, Luthy RG, Dzombak DA, Smith JR (2004) Release of polychlorinated biphenyls from river
sediment to water under low-flow conditions: Laboratory assessment. Journal of
Environmental Engineering-Asce 130:126-135
Perus J, Bonsdorff E (2004) Long-term changes in macrozoobenthos in the Åland archipelago, northern
Baltic Sea. Journal of Sea Research 52:45-56
Petersen K, Kristensen E, Bjerregaard P (1998) Influence of bioturbating animals on flux of cadmium
into estuarine sediment. Marine Environmental Research 45:403-415
Pignatello JJ, Xing BS (1996) Mechanisms of slow sorption of organic chemicals to natural particles.
Environmental Science & Technology 30:1-11
Presley BJ (1971) Techniques for analyzing interstitial water samples. Part I: Determination of selected
minor and major inorganic constituents. Initial Report of Deep Sea Drilling Project 7:17491755
Rasmussen E (1973) Systematics and ecology of the Isefjord marine fauna (Denmark). Ophelia 11:1-507
Reise K (2002) Sediment mediated species interactions in coastal waters. Journal of Sea Research
48:127-141
Riedel GF, Sanders JG, Osman RW (1987) The effect of biological and physical disturbances on the
transport of arsenic from contaminated Estuarine sediments. Estuarine Coastal and Shelf
Science 25:693-706
Riedel GF, Sanders JG, Osman RW (1997) Biogeochemical control on the flux of trace elements from
estuarine sediments: Water column oxygen concentrations and benthic infauna. Estuarine
Coastal and Shelf Science 44:23-38
Riisgård HU, Larsen PS (2005) Water pumping and analysis of flow in burrowing zoobenthos: an
overview. Aquatic Ecology 39:237-258
Rosenberg R (2001) Marine benthic faunal successional stages and related sedimentary activity. Scientia
Marina 65:107-119
Rumohr H, Bonsdorff E, Pearson TH (1996) Zoobenthic succession in Baltic sedimentary habitats.
Archive of Fishery and Marine Research 44:179-213
- 36 -
Sandnes J, Forbes T, Hansen R, Sandnes B (2000) Influence of particle type and faunal activity on
mixing of di(2-ethylhexyl)phthalate (DEHP) in natural sediments. Marine Ecology-Progress
Series 197:151-167
Santschi PH, Lenhart JJ, Honeyman BD (1997) Heterogeneous processes affecting trace contaminant
distribution in estuaries: The role of natural organic matter. Marine Chemistry 58:99-125
Scaps P (2002) A review of the biology, ecology and potential use of the common ragworm Hediste
diversicolor (OF Muller) (Annelida : Polychaeta). Hydrobiologia 470:203-218
Schneider AR, Porter ET, Baker JE (2007) Polychlorinated biphenyl release from resuspended Hudson
River sediment. Environmental Science & Technology 41:1097-1103
Schwarzenbach RP, Gschwend PM, Imboden DM (2003) Environmental organic chemistry, Vol. John
Wiley & Sons, Inc.
Stips A, Prandke H, Neumann T (1998) The structure and dynamics of the bottom boundary layer in
shallow sea areas without tidal influence: an experimental approach. Progress in
Oceanography 41:383-453
Thibodeaux LJ, Valsaraj KT, Reible DD (2001) Bioturbation-driven transport of hydrophobic organic
contaminants from bed sediment. Environmental Engineering Science 18:215-223
Wang QR, Kim D, Dionysiou DD, Sorial GA, Timberlake D (2004) Sources and remediation for
mercury contamination in aquatic systems - a literature review. Environmental Pollution
131:323-336
Wania F, Daly GL (2002) Estimating the contribution of degradation in air and deposition to the deep
sea to the global loss of PCBs. Atmospheric Environment 36:5581-5593
Weston DP, Maruya KA (2002) Predicting bioavailability and bioaccumulation with in vitro digestive
fluid extraction. Environmental Toxicology & Chemistry 21:962-971
Worms I, Simon DF, Hassler CS, Wilkinson KJ (2006) Bioavailability of trace metals to aquatic
microorganisms: importance of chemical, biological and physical processes on biouptake.
Biochimie 88:1721-1731
Zettler ML, Bick A, Bochert R (1995) Distribution and population-dynamics of Marenzelleria viridis
(Polychaeta, Spionidae) in a costal water of the Southern Baltic. Archive of Fishery and
Marine Research 42:209-224
Zettler ML (1996) Successful establishment of the spionid polychaete, Marenzelleria viridis (Verrill,
1873), in the Darss-Zingst estuary (southern Baltic) and its influence on the indigenous
macrozoobenthos. Archive of Fishery and Marine Research 43:273-284
Zettler ML, Daunys D, Kotta J, Bick A (2002) History and success of an invasion into the Baltic Sea:
The polychaete Marenzelleria cf. viridis, development and strategies. Invasive Aquatic
Species of Europe:66-75
- 37 -